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Ecology of Freshwater Fish 2013
Published 2013. This article is a U.S.
Government work and is in the public domain in the USA.
ECOLOGY OF
FRESHWATER FISH
Longer food chains and crowded niche space:
effects of multiple invaders on desert stream food
web structure
Timothy E. Walsworth1,*, Phaedra Budy1,2, Gary P. Thiede1
1
Department of Watershed Sciences, Utah State University, Logan, UT 84322, US
U.S. Geological Survey Utah Cooperative Fish and Wildlife Research Unit, Utah State University, Logan, UT 84322, US
2
Accepted for publication January 19, 2013
Abstract – Tributaries of the Colorado River Basin, historically home to a complex of endemic omnivores
collectively referred to as the ‘three species’; flannelmouth sucker (Catostomus latipinnis), bluehead sucker
(C. discobolus) and roundtail chub (Gila robusta), have experienced the establishment of numerous non-native fish
species. In this study, we examine the impacts of the trophic ecology of non-native fishes on the ‘three species’ in
the San Rafael River, Utah, USA. We employ a suite of abundance comparisons, stable isotope techniques and
size-at-age back-calculation analyses to compare food web structure and growth rates of the ‘three species’ in study
areas with and without established populations of non-native species. We found that the ‘three species’ are more
abundant in areas with few non-native fishes present, regardless of habitat complexity. Stable isotope analyses
indicate non-native fishes lengthen the food chain by 0.5 trophic positions. Further, the trophic niche spaces of the
native fishes shift and are narrower in the presence of non-native fishes, as several non-native species’ trophic niche
spaces overlap almost entirely with each of the ‘three species’ (bluehead sucker and flannelmouth sucker 100%,
roundtail chub 98.5%) indicating strong potential for competition. However, the ‘three species’ demonstrated no
evidence of reduced growth in the presence of these non-native fishes. Collectively, these results suggest that while
non-native fishes alter the food web structure presenting novel sources of predation and competition, mechanisms
other than competition are controlling the size-structure of ‘three species’ populations in the San Rafael River.
Key words: non-native species; competition; novel predators; growth; stable isotope analysis
Introduction
The impact of human development increasingly
threatens the native biodiversity of freshwater ecosystems (Ricciardi & Rasmussen 1999; Dudgeon et al.
2006). Anthropogenic alterations to rivers result in
physical (e.g., flow alteration, sedimentation, channelisation), chemical (e.g., pollution, nutrient loading)
and biological (e.g., invasive species, disease) degradation of natural habitats. These alterations can
favour novel life-history strategies (Olden et al.
2006), decrease resource availability (Tyus & Karp
1990; Brouder 2001), alter the flow of energy
through ecosystems (Sousa et al. 2008) and increase
predation and competition pressure on native species
(Tyus & Saunders 2000). As such, anthropogenic
alterations can result in new evolutionary and
contemporary pressures on native biota that evolved
under a specific suite of environmental conditions,
often dramatically restructuring communities.
Biotic communities are structured not only by the
environmental tolerances of the species present, but
also by interactions among the species of the community. Interspecific competition for resources can limit
growth and survival of inferior competitors (e.g.,
Schoener 1983) and thus limit the distribution and
abundance of species. However, negative populationlevel effects resulting from competition have proven
Correspondence: Timothy E. Walsworth, Department of Watershed Sciences, Utah State University, Logan, UT 84322. E-mail: [email protected]
*
Current address: School of Aquatic and Fishery Sciences, University of Washington,Box 355020, Seattle WA 98195
doi: 10.1111/eff.12038
1
Walsworth et al.
difficult to detect in many, though not all, studies
(reviewed in Connell 1983). In addition, predator
species can have a particularly strong role in shaping
community structure through both direct (e.g., Kitchell et al. 1997) and indirect pathways (e.g., Werner
et al. 1983; Romare & Hansson 2003). Alterations to
trophic structure, such as the establishment of nonnative species, can have significant impacts on community structure (e.g., Reissig et al. 2006). However,
the impact of invasive predators and competitors is
not consistent for all recipient systems and is influenced by ecosystem complexity (Case 1990; Carey &
Wahl 2010, 2011) and evolutionary history (Kitchell
et al. 1997; Shea & Chesson 2002).
Rivers and streams of the Colorado River Basin,
home to a historically depauperate and highly endemic fish fauna, have been particularly affected by
anthropogenic disturbances (Minckley & Deacon
1968), due in part to the region’s arid climate and
rapidly expanding human population. While degradation of the physical environment is often argued to
be the primary cause of population and range reductions of native fishes (Ross 1986), interactions with
non-native fishes may be equally or even more influential than habitat loss in the extinction of species
(Tyus & Saunders 2000; Woodford 2009a). Invasion
by non-native fishes has the potential to alter the
energetic pathways of the historic food web, resulting
in significant and negative ecosystem impacts, such
as modified habitat coupling, nutrient cycling rates
and ecosystem resilience (Eby et al. 2006; Britton
et al. 2010; Pilger et al. 2010). Non-native species
often maintain a competitive advantage over native
fishes (Shea & Chesson 2002; Cox & Lima 2006)
and can have particularly strong impacts on simple
food webs (Carey & Wahl 2010), such as those of
the historical Colorado River Basin (Tyus & Nikirk
1990; Tyus & Saunders 2000; Unmack & Fagan
2004).
In addition, the interaction between a degraded
physical habitat and non-native species presence can
result in complex synergistic effects on native species
and their habitat (Brook et al. 2008). Physical habitat
degradation, for example, can aid in the establishment and dispersal of invasive species (Marvier et al.
2004). While change in flow regimes may decouple
the life histories of native fishes from their current
environmental template, many invasive fishes are
pre-adapted to the new conditions (Olden et al. 2006;
Johnson et al. 2008). In addition , the impact of nonnative fishes has been suggested to be strongest at
times of low flow (Pilger et al. 2010), a nearly
perpetual state in degraded desert rivers. This combination of physical degradation and biotic invasions in
the Colorado River Basin has contributed to the extirpation and the federal listing of many endemic fishes
2
under the Endangered Species Act (Minckley &
Deacon 1968; USDI, Fish & Wildlife Service 1994)
and the protection of many others under conservation
agreements between states of the Colorado River
Basin (UDWR, Utah Division of Wildlife Resources
2006).
The bluehead sucker (Catostomus discobolus),
flannelmouth sucker (C. latipinnis) and roundtail
chub (Gila robusta) represent a highly imperilled
ecological complex of fishes, hereafter, collectively
the ‘three species’, native to the upper Colorado
River Basin, U.S.A. These endemic fishes are listed
as state species of concern and subject to a rangewide conservation agreement aimed at ensuring their
persistence throughout their range (UDWR 2006).
Many of the non-native fishes present in the basin
have the potential to negatively impact populations of
these native fishes through competition or predation
(e.g., Bestgen & Propst 1989; Tyus & Saunders
2000; Johnson et al. 2008). In fact, predation on
early life stages of native fish by non-native fish has
been implicated in total recruitment failure for native
fishes in the Colorado River Basin and other systems
(Meffe 1985; Woodford 2009b).
Populations of imperilled species may be able to
persist in an area if recruitment cannot balance with
mortality, provided there is a source habitat capable
of supplying colonisers to the sink habitat (Pulliam
1988). Previous study has suggested that populations
of the ‘three species’ in the downstream, degraded
portions of the San Rafael River, a tributary of the
Green River, occupy a sink habitat, and are maintained through colonisation from sources in both the
upper portions of the San Rafael River and the
main-stem Green River (e.g., Bottcher 2009). Identification of the mechanisms (i.e., competition and/or
predation) by which non-native fishes interact with
the ‘three species’ may illuminate the causes of
source-sink structure. In this article, we address the
following questions: (i) do non-native fishes occupy
piscivorous trophic positions and/or change the trophic position occupied by native fishes and (ii) does
the presence of non-native fishes alter the growth of
native fishes? In addressing these questions, we
explore a combination of food web and growth analyses among patches of a river with alternate invasion histories to advance our understanding of how
trophic interactions impact community composition
and population structure.
Study area
The San Rafael River (hereafter ‘SRR’), Utah,
U.S.A., is an ideal study stream as it has experienced
degradation representative of many tributaries of the
Colorado River Basin (i.e., altered hydrograph, water
Effects of multiple invaders on imperiled desert fishes
loss, channelisation, homogenisation of habitat, invasive species establishment; Walker & Hudson 2004;
Bottcher 2009). The SRR drains 4500 km2 of southeastern Utah and is formed by the confluence of
Ferron, Cottonwood, and Huntington creeks (Fig. 1).
The SRR is a spring snowmelt and autumn monsoon
driven system, and flows approximately 175 km from
its headwaters in the Manti–La Sal National Forest to
its confluence with the Green River near the town of
Green River, Utah. The SRR is one of the most overallocated rivers in Utah (Walker & Hudson 2004)
and the lower 64 km are frequently dewatered during
the summer irrigation season (Bottcher 2009).
Native fish species currently occupying the SRR
for at least a portion of their life history include the
flannelmouth sucker, bluehead sucker, roundtail
chub, speckled dace (Rhinichthys osculus), as well as
occasional, transient bonytail (Gila elegans), razorback sucker (Xyrauchen texanus) and Colorado
pikeminnow (Ptychocheilus lucius). Non-native species present include red shiner (Cyprinella lutrensis),
sand shiner (Notropis stramineus), fathead minnow
(Pimephales promelas), channel catfish (Ictalurus
punctatus), black bullhead (Ameiurus melas), common carp (Cyprinus carpio), white sucker (Catostomus commersoni), green sunfish (Lepomis cyanellus)
and virile crayfish (Orconectes virilis).
In this study, we delineate the upper and lower SRR
by the San Rafael Reef, dividing the river into the section flowing through the San Rafael Swell, characterised by deep canyons (upper SRR), and the section
flowing through the San Rafael Desert, characterised
by primarily open desert terrain (lower SRR). Natural
and anthropogenic barriers in the San Rafael Reef and
at the Hatt Ranch diversion dam limit upstream movement of fishes. Twelve 300 m long sampling sites
were established in total (Fig. 1). The sites in the
upper SRR (N = 4) were chosen opportunistically due
to extremely rugged terrain, while sites in the lower
SRR (N = 8) were chosen by a systematic sample
design with random seed start (Bottcher 2009).
Methods
Collection of biotic community data
Sampling events occurred during the spring (i.e., prior
to spring snowmelt run-off; April and May), summer
(i.e., immediately after recession of spring runoff;
June and July) and autumn (i.e., October) of 2010.
Fish from all habitat types were sampled via canoe
electrofishing, and all native and non-native fishes
were identified to species, anesthetised with tricaine
methanosulphate (MS-222), weighed, measured for
total length and clipped (lower caudal fin) for stable
isotope analysis. Tissue samples were preserved and
stored in 95% ethanol until processing later in the lab,
and native fishes were fin-clipped for age determination (see below). Storing tissue samples in ethanol
has been shown to enrich d13C signatures in some
studies (Kaehler & Pakhomov 2001; Kelly et al.
2006), to have no significant effect in other studies
(Sarakinos et al. 2002; Serrano et al. 2008) and to
cause small shifts relative to ecological variation
(Kelly et al. 2006). We were confident using these
tissues given that all indices were relative and as long
as carbon signatures were interpreted with caution.
Following sample collection, native fishes were held
in a recovery tank until they showed no effects of the
anaesthetic before being returned to the river.
Benthic invertebrates were sampled at each food
web site with a Surber sampler. For each sampling
event, eight 0.09 m2 samples were taken from riffles
in each site. Samples within a site and date were
combined in 95% ethanol, returned to the lab where
they were sorted, identified to family (or lower) and
functional feeding group, and counted.
Relative abundance of native fishes in presence of
non-native species
Fig. 1. Map of the San Rafael River watershed. Inset shows
location of watershed (cross-hatched) in Utah, USA.
The sampling sites were placed into three categories
of degradation (Fig. 1). The high quality category
3
Walsworth et al.
(all located in the upper SRR) had widely available
complex habitat (i.e., riffles, pools and backwaters)
and very low to zero densities of non-native fishes
present. The medium quality category (all located in
the lower SRR, with one site upstream of the Hatt
Ranch diversion dam, yet downstream of the San
Rafael Reef) had widely available complex habitat,
but high densities of non-native fishes present. The
poor quality category (all in the lower SRR) all had
very limited complex habitat available and high densities of non-native fishes. Habitat complexity was
calculated as the per cent of the reach consisting of
riffle, pool or backwater habitat as determined by
in-stream habitat surveys (Walsworth 2011). While
the surrounding terrain is somewhat different between
the upper and lower SRR (Fortney et al. 2011), the
in-stream habitat in high and medium quality reaches
was similar. A repeated measures analysis of variance, repeated on sampling site, was run to compare
the catch-per-unit-effort (CPUE) of native fishes and
of non-native fishes between sites in the different
quality categories.
Stable isotope analysis of food web structure
Once returned to the lab, caudal fin clips and benthic
invertebrates of the collector-filterer functional feeding groups (most abundant) were prepared for stable
isotope analysis. Tissue samples were dried for 48 h
at 70 °C, crushed into a homogeneous powder with
mortar and pestle and placed in tin capsules for shipment. To examine the effect of non-native species on
the trophic structure of the SRR, samples from the
upper SRR (high quality sites) and from the lower
SRR (medium and poor quality sites) were analysed
for stable isotopic signatures separately. We chose
this division due to the results of our repeated measures ANOVA, as it separated areas of the river with
(lower SRR) and without (upper SRR) abundant
non-native fishes. When possible, we collected a
minimum of 10 samples from each species in both
the upper and lower SRR (Vinson & Budy 2011).
Capsules were sent to the Washington State University Stable Isotope Core Lab (Pullman, WA) for
natural abundance analyses of 13C and 15N. Isotopic
signatures are reported in d-notation:
d C or d N ¼
13
15
Rsample
1 1000;
Rstandard
where R is the ratio of 13C/12C or 15N/14N. The standard for d13C is PeeDee belemnite and for d15N is
atmospheric nitrogen. The stable isotopic signatures
of the collector-filterer invertebrate group were used
as a baseline to allow comparison between different
4
sites along the longitudinal gradient of the SRR, as
this was the only functional group of invertebrates
consistently collected in Surber samples. Collectorfilterer insects accounted for a median of 88.6%
(mean = 76.4%; SE = 3.7%; Skewness = 1.47) of
Surber sample composition. The primary collector-filterer families collected and analysed in this study
were Hydropsychidae (Order: Trichoptera) and Simuliidae (Order: Diptera). Families were analysed for
stable isotope signature separately, and the results
were combined to measure the mean collector-filterer
signature. Each of these families was found in both
the upper and lower SRR.
Carbon and nitrogen isotope signatures were corrected for basal resource variation before further analysis. Carbon signatures were corrected using the
following equation:
d13 Ccor ¼
d13 Ci d13 Cmeancf
CRcf
where d13Ci is the carbon isotope signature of organism i, d13Cmeancf is the mean collector filterer carbon
isotopic signature from the site where organism i was
collected and CRcf is the carbon range of the same
collector filterer invertebrates as above (Olsson et al.
2009). Nitrogen values were corrected (d15Ncor) for
baseline variation by:
d15 Ncorj;i ¼ d15 Nj;i d15 Ncf ;i d15 Ncf ; min
where d15Nj,i is the nitrogen signature of sample j at
site i, d15 Ncf ;i is the mean d15N of collector-filterers
at site i, and d15 Ncf ;min is the minimum mean collector-filterer d15N of all sites (adapted from Cabana &
Rasmussen 1996 to display stable isotope signatures
in d-space). Although baseline signatures differed
between individual sampling sites (d13C SD = 1.05,
d15N SD = 1.1), we did not detect any longitudinal
patterns in carbon or nitrogen baselines. Due to heterogeneous catch rates associated with their low abundance and imperilled status, a subsample of
individuals captured at sites with high catch rates
were analysed for stable isotope signatures to characterise the food web structure throughout the upper
and lower SRR. Due to limited sample sizes for the
‘three species’, especially in the lower SRR, stable
isotope data were pooled across seasons (spring, summer, and autumn).
Species’ trophic niche space was analysed using
methods presented in Layman et al. (2007). For each
species, the following measures were calculated; trophic position (TP), nitrogen range (NR), carbon range
Effects of multiple invaders on imperiled desert fishes
(CR), trophic niche width, trophic niche overlap and
food chain length. Trophic position was calculated
using the following equation:
TPi ¼
d15 Ncori d15 Ncorcf
þ 2;
3:4
where TPi is the trophic position of species i, Ncori is
the corrected nitrogen signature of species i, and
Ncorcf is the corrected nitrogen signature of collector
filterer invertebrates (Vander Zanden & Rasmussen
1999). Collector-filterer invertebrates were assumed to
have a trophic position of 2 and we assumed trophic
fractionation of d15N to be 3.4& as trophic level
increases (Minagawa & Wada 1984). Trophic position
and d13Ccor signatures for each of the ‘three species’
were compared between the upper and lower SRR
with Student’s t-tests. Nitrogen range and carbon
range were calculated from the following equations:
NR ¼ d15 Ncormax d15 Ncormin ;
CR ¼ d13 Ccormax d13 Ccormin
for each species (Layman et al. 2007). Niche width
was calculated as the convex hull area of isotopic signatures of each species plotted in C-N bivariate space
(Layman et al. 2007). Niche overlap was calculated
as the per cent of a species’ niche width area that is
overlapped by the niche width area of another species
in the food web. Food chain length was calculated as
the highest TP detected in the upper or lower SRR.
Calculation of native fish growth rates
The basal portion of the second dorsal fin ray was
collected from each individual of the ‘three species’
captured during sampling, and stored in vials until
returned to the lab. The fin rays were placed in molds
and heated at 70 °C for 12 h to allow the mold to
harden. The molds were then mounted on metal
chucks and cut using a Buehler Isomet low-speed
saw (Buehler Ltd., Lake Bluff, IL, USA). The fresh
edge was sanded, polished and a second cut was
made to produce a thin (~1.5 mm) section. The section was placed on a microscope slide and polished if
necessary. Fin ray sections were placed under a camera-mounted microscope and back-lit to reveal annuli.
Digital images of each section were captured and
analysed for length-at-age using the Frasier-Lee
back-calculation:
St
Lt ¼ c þ ðLT cÞ
ST
where Lt is the length of the fish at time t, LT is the
total length of the fish, c is the length of the fish at
age 1, St is the length of the fin ray at time t and ST
is the total length of the fin ray (Francis 1990). The
length of each species at age 1 (c) was estimated
from length-frequency plots. Length-at-age data for
each species were then fit to a repeated measures
non-linear Von Bertalanffy growth curve (VBGC;
Jones 2000):
Lt ¼ L1 1 ek ðt t0 Þ
where L∞ represents the maximum possible length
achieved by the fish, Lt is the fish’s length at time t,
t0 is the theoretical age of the fish when its length
equals zero and k is the Brody growth rate coefficient
(Ricker 1975), a measure of the rate of approach to
L∞. Growth rates of fish in the upper and lower SRR
were examined by comparing the standardised residuals from the VBGC of individual fish captured in
each section. A Student’s t-test was used to compare
the residuals between groups. All statistical analyses
were run in the R Statistical Environment (R Development Core Team 2011) with an a priori a of 0.05.
Results
Relative abundance
The lower SRR fish community species composition
was dominated by non-native fishes, while the fish
collections in the upper SRR were almost entirely
composed of native fishes (Table 1). In addition,
juvenile individuals of the ‘three species’ were
uncommon in the electrofishing samples (Table 1).
The ‘three species’ were captured in significantly
greater numbers in the high-quality sites (CPUE
= 26.22 3.69 fish per hour [mean 1.96∙SE])
than in either the medium (CPUE = 3.93 1.14 fish
per hour) or low-quality sites (CPUE = 4.30 1.04
fish per hour; repeated measures ANOVA, P = 0.001;
Fig. 2a), while non-native fishes were captured in
significantly greater numbers in both the medium
(CPUE = 61.01 11.60 fish per hour) and low(CPUE = 53.09 6.13 fish per hour) quality sites
than in the high-quality sites (CPUE = 0.79 0.46
fish per hour; repeated measures ANOVA P < 0.001;
Fig. 2b). No significant seasonal or interaction effects
were detected for CPUE of either native or nonnative fishes (all repeated measures ANOVA P > 0.05).
The only non-native fishes captured upstream of the
San Rafael Reef were 2 green sunfish and 1 Utah
chub (Gila atraria). Non-native white sucker were
captured in the lower SRR for the first time in 2010.
The relative abundances of benthic invertebrates
were not significantly different between the upper
and lower SRR (ANOVA, P = 0.432). When compar5
Walsworth et al.
Table 1. Number and mean, minimum (‘Min’) and maximum (‘Max’) total lengths of individuals sampled in the San Rafael River by species and location. Cells
with no data available marked with ‘–’.
Upper San Rafael River
Species
Native Species
Age-0 sucker
Bluehead sucker (BHS)
Flannelmouth sucker (FMS)
Roundtail chub (RTC)
Speckled dace (SDD)
Non-native Species
Black bullhead (BBH)
Channel catfish (CLC)
Common carp (CNC)
Fathead minnow (FHM)
Green sunfish (GNS)
Red shiner (RDS)
Sand shiner (SDS)
Utah chub
White sucker (WES)
Native Species
CPUE (fish hr–1)
60
Lower San Rafael River
N
Mean
Length
Min
Length
Max
Length
N
Mean
Length
Min
Length
Max
Length
18
155
110
40
321
26.7
178.9
284.7
145.2
63.9
21
75
106
55
29
38
290
426
261
98
37
16
25
21
15
25.9
214.0
191.8
180.2
70.9
18
176
117
74
60
32
260
325
290
97
0
0
0
0
2
0
0
1
0
–
–
–
–
95.5
–
–
135.0
–
–
–
–
–
51
–
–
135
–
–
–
–
–
140
–
–
135
–
7
16
6
28
15
453
711
0
4
188.6
248.3
451.0
66.0
118.9
55.8
52.6
–
166.8
140
60
407
54
69
20
15
–
120
235
384
511
74
165
84
94
–
220
ing only densities of collector filterer insects only,
there was still no significant difference between the
upper and lower SRR (ANOVA, P = 0.319).
(a)
50
40
Stable isotope analysis
30
The upper SRR can be broadly characterised by a
short food chain (food chain length = 3.51; Table 2,
Fig. 3a) and food web populated by few species. The
bluehead
sucker
(‘BHS’,
TP = 2.75 0.18
[mean 1.96∙SE]), flannelmouth sucker (‘FMS’,
TP = 2.95 0.22) and roundtail chub (‘RTC’,
TP = 2.80 0.24) occupied similar trophic positions
(ANOVA P = 0.38) that signify the assimilation of benthic invertebrates. The ‘three species’ displayed significantly different d13Ccor signatures (BHS d13Ccor
= 0.65 0.18; FMS d13Ccor = 0.77 0.24; RTC
d13Ccor = 1.91 0.40; ANOVA P < 0.001). The bluehead sucker was more depleted in carbon than either
the flannelmouth sucker (t-test P < 0.001) or the
roundtail chub (t-test P < 0.001), and the flannelmouth sucker was more depleted in carbon signature
than the roundtail chub (t-test P < 0.001). Speckled
dace occupied the highest mean trophic position in
the upper SRR (TP = 3.18 0.08) and demonstrated
an intermediate d13C signature among the upper SRR
fish community (d13Ccor = 0.64 0.59).
While the food web of the upper SRR was structurally simple, the food web of the lower SRR was
populated by more species distributed across a
broader range of trophic positions (food chain
length = 4.01; Table 2, Fig. 3b). As in the upper
SRR, the bluehead sucker (TP = 2.82 0.06) and
flannelmouth sucker (TP = 2.84 0.06) occupied
20
10
0
High
Medium
Poor
Reach quality
Non-native Species
CPUE (fish hr–1)
150
(b)
125
100
75
50
25
0
High
Medium
Poor
Reach quality
Fig. 2. Catch-per-unit-effort (fish/hr) of native (a) and non-native
(b) fish in the San Rafael River by site quality. The high-quality
sites have significantly greater CPUE of native fishes (ANOVA
P = 0.001) and significantly lower CPUE of non-native fishes
(ANOVA P < 0.001) than either the medium or poor quality sites.
6
Effects of multiple invaders on imperiled desert fishes
Table 2. Stable isotope signatures by species and location in the San Rafael River. Sample size (N), mean corrected stable isotope signature values and
standard errors are reported. Cells with no data available marked with ‘–’.
Upper San Rafael River
Species
Native Species
Collector-Filterer Insects(ColFil)
Bluehead sucker (BHS)
Flannelmouth sucker (FMS)
Roundtail chub (RTC)
Speckled dace (SDD)
Non-native Species
Black bullhead (BBH)
Channel catfish (CLC)
Common carp (CNC)
Fathead minnow (FHM)
Green sunfish (GNS)
Red shiner (RDS)
Sand shiner (SDS)
White sucker (WES)
15
N
d Ccor (SE)
d Ncor (SE)
N
d13Ccor (SE)
d15Ncor (SE)
18
10
10
9
5
0.00 (0.09)
0.53 (0.06)
0.77 (0.12)
1.91 (0.20)
0.64 (0.30)
3.53 (0.12)
6.14 (0.36)
6.74 (0.37)
6.26 (0.39)
7.54 (0.14)
81
10
11
10
0
0.00 (0.04)
1.26 (0.09)
2.02 (0.19)
2.38 (0.31)
–
3.53
6.33
6.39
7.78
–
(0.06)
(0.12)
(0.12)
(0.41)
0
0
0
0
0
0
0
0
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
4
10
5
7
7
37
28
4
1.84 (0.47)
2.68 (0.35)
1.47 (0.39)
0.90 (0.07)
1.81 (0.25)
1.04 (0.15)
1.82 (0.23)
2.01 (0.67)
8.45
8.32
5.84
7.53
8.79
6.89
7.37
6.27
(0.33)
(0.23)
(0.68)
(0.43)
(0.42)
(0.10)
(0.13)
(0.38)
(a)
10
δ15Ncor
Lower San Rafael River
13
8
SDD
●
BHS
6
4
●
FMS
●
●
−2
−1
●
RTC
ColFil
0
1
2
3
4
13
δ Ccor
10
(b)
BKB
GNS
δ15Ncor
●
8
FHM
●
●
●
CLC
SDS
●
●
RTC
RDS
●
FMS
BHS ●
●
●
●
WES
CNC
6
4
●
−2
−1
0
ColFil
1
2
3
4
13
δ Ccor
Fig. 3. Stable isotope signatures (mean values 1.96 SE) and
food web structure of the upper (a) and lower (b) San Rafael
River. The ‘three species’ icons are enlarged. Mean values 1.96
SE shown. See Table 2 for abbreviations.
similar trophic positions (t-test P = 0.70), and the
two species demonstrated significantly different carbon signatures (BHS d13Ccor = 1.26 0.18; FMS
d13Ccor = 2.02 0.37; t-test P = 0.002). The roundtail chub had a significantly elevated trophic position
(TP = 3.34 0.27) in the lower SRR compared to
the two native suckers (ANOVA P < 0.001), and was
significantly elevated from its trophic position in the
upper SRR (t-test P = 0.009). The bluehead sucker
and flannelmouth sucker carbon signatures were significantly enriched in the lower SRR compared to the
upper SRR (both t-tests P < 0.001). All remaining
stable isotope measures for the ‘three species’ were
similar between the upper and lower SRR (t-tests, all
P > 0.05). Green sunfish held the highest trophic
position in the lower SRR (TP = 3.54 0.24), and
five other non-native species occupied higher trophic
positions than at least two of the ‘three species’.
The stable isotope signatures of fishes in the upper
SRR spanned a broad array of carbon sources and
trophic positions (CR = 3.71, NR = 4.08, niche
width = 12.79). Bluehead sucker occupied a narrow
trophic niche (CR = 0.53, NR = 3.37, niche
width = 6.96; Fig. 4a), aligning closely with collector-filterer insects with respect to carbon signature.
The bluehead sucker niche space did not overlap with
other native species trophic niches.. Flannelmouth
sucker had a slightly wider, less distinct, trophic
niche space than the bluehead sucker (FMS
CR = 1.27, NR = 3.24, niche width = 7.14, overlap = 22.4%). The roundtail chub occupied the widest trophic niche space out of the ‘three species’ in
the upper SRR, and had less niche overlap than the
flannelmouth sucker (CR = 1.89, NR = 3.32, niche
width = 8.41, overlap = 6.9%).
The stable isotope signatures of fishes in the lower
SRR was similar to that used in the upper SRR,
although a slightly wider range of trophic positions
were inhabited and there was greater variation in
resource use at all given trophic positions
(CR = 5.15, NR = 4.96, niche width = 18.12;
Fig. 4b). Bluehead sucker trophic niche space in the
7
Walsworth et al.
lower SRR was much narrower and less distinct than
in the upper SRR (CR = 0.77, NR = 1.21, niche
width = 3.25, overlap = 100%). Flannelmouth sucker
trophic niche space was also considerably more narrow and less distinct than in the upper SRR
(CR = 1.89, NR = 1.22, niche width = 5.03, overlap = 100%). Roundtail chub trophic niche space
was slightly wider in the lower SRR (CR = 2.95,
NR = 3.69, niche width = 9.89), but was overlapped
with other species’ trophic niche spaces to a much
greater degree (overlap = 98.5%) than in the upper
SRR. Red shiners, sand shiners, channel catfish, common carp and white suckers each occupied a trophic
niche that overlapped substantially with those of the
‘three species’.
Growth
The oldest bluehead suckers (age = 6 year) were captured in the upper SRR, while those captured in the
lower SRR had a greater mean age than those
captured in the upper SRR (lower SRR mean
12
(a)
δ15Ncor
10
8
6
age = 4.27 year, upper SRR mean age = 4.00 year).
Flannelmouth sucker and roundtail chub attained the
same maximum age measured in the SRR (maximum
age = 8 year). Flannelmouth sucker in the upper
SRR exhibited an older maximum age (8 year) measured, as well as an older mean age (5.07 year) than
those aged in the lower SRR (maximum = 7 year;
mean = 4.39 year). The lower SRR exhibited both
the oldest individual (8 + year) and a greater mean
roundtail chub age (4.59 year) than the upper SRR
(4.20 year). More individuals were analysed for age
and growth than were analysed for stable isotope signature (Upper SRR BHS N = 43, FMS N = 31, RTC
N = 10; Lower SRR: BHS N = 15, FMS N = 23,
RTC N = 17).
Flannelmouth sucker demonstrated the greatest
model-estimated maximum length (L∞ = 481.46 mm;
Fig. 5) and roundtail chub the smallest model-estimated maximum length (L∞ = 267.00 mm) of the
‘three species’. Bluehead sucker exhibited the greatest Brody growth rate coefficient (k = 0.21) and flannelmouth sucker the lowest predicted Brody growth
rate coefficient (k = 0.19). No differences in lengthat-age were detected between fish captured in the
upper and lower SRR for either flannelmouth sucker
(t-test P = 0.72) or roundtail chub (t-test P = 0.48).
However, bluehead sucker captured in the lower SRR
were significantly larger at age than those captured in
the upper SRR (t-test P = 0.012).
4
2
−2
0
2
4
13
12
(b)
δ15Ncor
10
8
6
4
2
−2
0
2
4
13
δ Ccor
Fig. 4. Trophic niche spaces occupied by fish species in the
upper (a) and lower (b) San Rafael River. The ‘three species’ are
shown with solid lines. Solid lines: blue = bluehead sucker,
green = flannelmouth sucker and yellow = roundtail chub;
Dashed lines: blue = sand shiner, red = red shiner, grey = channel catfish, yellow = green sunfish, light blue = fathead minnow,
black = collector filterer insects; Dotted lines: yellow = common
carp, red = white sucker, black = black bullhead; Dash-dotted
lines; red = speckled dace.
8
Backcalculated length (mm)
δ Ccor
600
500
400
300
200
100
0
350
300
250
200
150
100
50
0
300
250
200
150
100
50
0
(a)
●
●
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(b)
●
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(c)
●
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0
1
2
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3
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4
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5
6
7
8
Age
Fig. 5. Size-at-age with Von Bertalanffy growth function for flannelmouth sucker (a), bluehead sucker (b), and roundtail chub (c)
in the San Rafael River. Black triangles represent fish captured in
the lower San Rafael River; grey circles represent fishes captured
in the upper San Rafael River. Note different y-axes.
Effects of multiple invaders on imperiled desert fishes
Discussion
In this study, we analysed stable isotope signatures
and growth (a fitness-related measure) to examine
the effect of non-native species on trophic status and
growth of populations of imperilled desert fishes.
Our analysis of catch rates between areas with and
without complex habitat and non-native fishes
revealed that areas of the San Rafael River without
non-native fishes held significantly greater abundances of the ‘three species’ than those areas with
non-native species present, regardless of habitat quality. Results of the stable isotope analysis revealed
that non-native fish species have significantly altered
food web structure in the San Rafael River. After
detecting these changes to the trophic structure of
the river, we examined the relative growth and condition of the ‘three species’ to determine whether the
establishment of the non-native fish populations has
had an effect on the relative fitness of these
imperilled native fishes. Greater understanding of
these issues is critical to the effective conservation
and management of these endemic species, and has
implications for the conservation of species threatened by habitat loss and non-native species introductions worldwide.
Non-native species can alter the flow of nutrients
and energy through an ecosystem through alteration
of the number and strength of trophic linkages in a
food web (Eby et al. 2006; Sousa et al. 2008; Britton
et al. 2010). In the process, they may also facilitate
the establishment of other non-native species (Simberloff & Von Holle 1999). The stable isotope signatures of the ‘three species’ detected in this study
indicate trophic levels consistent with the diets
observed in previous studies (Childs et al. 1998; Bezzerides & Bestgen 2002; Quist et al. 2006). The
establishment of non-native fishes has increased the
number of resident fish species in the food web from
four in the upper San Rafael River (and assumed preinvasion lower San Rafael River) to eleven (including
seven non-native) species in the lower San Rafael
River. Although the food web of the upper San
Rafael River consists primarily of a few native, secondary consumers (the ‘three species’ and speckled
dace), the food web of the lower San Rafael River
consists of a crowded level of secondary consumers,
as well as a diverse level of tertiary consumers.
Acknowledging that the potential ecological impact
of an invading species is context dependent (i.e., on
the abiotic conditions and biotic community of the
invaded ecosystem; Ruesink 2003), the high diversity
of invading species in the San Rafael River increases
the likelihood that at least one of the established
non-native species will be a high-impact invader
(Ricciardi & Kipp 2008).
Due to the inherent isolation and insularity of
rivers and lakes, freshwater ecosystems often display
high rates of endemism (Dudgeon et al. 2006). Ecosystems comprised of highly endemic faunas, such as
streams in the Colorado River Basin, are more likely
to be negatively impacted by invading species, as the
invader often represents a novel predator or competitor archetype (Ruesink 2003; Cox & Lima 2006). In
isolation, prey species may not evolve defences (e.g.,
behavioural or morphological) against predators not
native to their range (Ruesink 2003), and often experience strong negative effects of introduced
non-native predators (Kitchell et al. 1997). Three
non-native fishes in the lower San Rafael River (i.e.,
channel catfish, black bullhead and green sunfish)
have trophic positions indicative of at least partial
piscivory. While previous studies suggest the largebodied piscivore trophic niche was occupied seasonally by endangered Colorado pikeminnow in Colorado River tributaries (Tyus & Saunders 2000;
Bottcher et al. in press), the established populations
of channel catfish, black bullhead and green sunfish
present a novel, year-round source of predation pressure for juveniles of the ‘three species’. Our limited
catches of juveniles in the river suggest that they
occur at low abundances, are highly patchy in
distribution, or are less susceptible to our sampling
methods. Additional samples with a stick seine in
backwater and slow, marginal habitats also had very
limited catches of juveniles, suggesting that gear bias
was not the cause of the limited catch numbers. Red
shiners have been shown to be significant predators
on larval and juvenile stages of Colorado River fishes
(Tyus & Nikirk 1990; Tyus & Saunders 2000). While
we argue that novel predators likely have substantial
negative effects on juveniles of the ‘three species’,
our data show that more juveniles of the ‘three species’ were captured in the lower San Rafael River
than were captured in the upper San Rafael River.
This occurrence is likely due to the habitat characteristics of the sampling sites in the upper San Rafael,
which, while having extensive complex habitat, did
not have backwater habitats, the preferred habitats of
juvenile native fishes, available. The contemporary
suite of novel predator archetypes in the river
presents the potential for substantial impacts on the
recruitment success and viability of the ‘three
species’ (Meffe 1985).
In addition to the negative effects of predation
from invasive species, these invaders may also compete with native species for resources. Competition
for resources can be demonstrated by a numerical
response (Pell & Tidemann 1997), a shift in resource
usage (Werner & Hall 1979; Davey et al. 2006),
change in morphology (Crowder 1984), and/or a
change in vital rates in the presence of potential com9
Walsworth et al.
petitors (Davey et al. 2006). Competition cannot be
inferred from stable isotope signatures alone (Newsome et al. 2007), as multiple combinations of basal
resources and prey items can result in similar isotopic
signatures. Nonetheless, our trophic niche space analysis suggests that the presence of numerous nonnative species in the lower San Rafael River has the
potential to increase competition for food resources
for the ‘three species’ (DeNiro & Epstein 1978; Zambrano et al. 2010). The vast majority of the trophic
niche space of each of the ‘three species’ is overlapped by multiple non-native fishes. Furthermore,
the trophic niches of the bluehead sucker and
flannelmouth sucker are altered in the presence of
non-native fishes. In the lower San Rafael River, both
species demonstrated a more enriched d13C signature
than in the upper San Rafael River, potentially indicative of a shift from riffle to more pool-derived
resources (Finlay et al. 2002). It is important to note,
however, that this shift in carbon signature could
result from competitive exclusion by the non-native
fishes, the scarcity of riffle habitats in the degraded
lower San Rafael River, or some combination of
both. The reduction in the range of nitrogen signatures demonstrated by both bluehead sucker and flannelmouth sucker may be indicative of niche
displacement whereby non-native species are limiting
the native fishes’ food resource use to lower trophic
level items, potentially through exploitative competition over the resource or interference competition relegating the native species to less preferred habitats
(Douglas et al. 1994).
As resources become concentrated into smaller
areas, competition can intensify over an increasingly
limited resource pool (Mills et al. 2004), reducing the
energy available to native species. Competition-based
changes to a fish’s energy intake (i.e., quantity or
quality) can result in less favourable growth patterns,
as the fish may not be able to obtain necessary
resources, or may have to increase energy expenditure to feed (Mills et al. 2004; Davey et al. 2006).
Decreased growth rates can negatively affect fish
populations, as fecundity (Bagenal 1978), age-atmaturity (Alm 1959), and, often, survival (Quinn &
Peterson 1996) are strongly correlated with body size.
For example, faster growth rates can enable fish to
escape gape-limited predators and avoid starvation
during extreme environmental conditions (Post &
Evans 1989; Quinn & Peterson 1996). However, the
‘three species’ do not demonstrate lower growth rates
in the lower San Rafael River relative to the upper
San Rafael River, even in the face of lesser resource
abundance (Walsworth 2011) and greater potential
for competition. Previous studies have suggested that
source-sink dynamics control the populations of the
‘three species’ in the San Rafael River (Bottcher
10
2009), with the upper San Rafael River and the
main-stem Green River providing colonists to
the lower San Rafael sink habitat. The ‘three species’
are each highly mobile species that make long distance movements in both downstream and upstream
directions, either through larval drift or directed adult
migration (e.g., Chart & Bergersen 1992; Robinson
et al. 1998; Compton et al. 2008). Movement of individuals from the Green River into the San Rafael
River could mask any differences in growth resulting
from competition. Flannelmouth sucker and bluehead
sucker have been shown to grow faster and to larger
sizes in larger rivers (Sweet et al. 2009). In addition,
unidirectional movement downstream over the Hatt
Ranch diversion dam, a barrier to upstream movement, could mask any fitness-related effects of competition with non-native species in the lower river.
In addition to disrupting connectivity, dams and
diversions often result in more stable flow regimes.
In a static environment, Menge & Sutherland (1987)
predicted that the effect of predation outweighs the
effects of competition or physical factors on intermediate level consumers, such as the ‘three species’,
especially in systems with high levels of omnivory.
The highly altered contemporary flow regime of the
San Rafael River has led not only to habitat homogenisation, but also to frequent low flow and dewatering events (Bottcher 2009). Predation should have a
stronger impact on populations in homogeneous habitat (Caroffino et al. 2010) and at times of low flow
(Pilger et al. 2010), as the fish are concentrated into
smaller habitat areas with less refuge. The lack of
significant growth differences in the San Rafael
River, coupled with the greater abundances of the
‘three species’ in the upper San Rafael River, regardless of habitat quality, suggest that predation by the
non-native fishes in the lower river has a stronger
impact on the ‘three species’ than does greater competition for resources, similar to the findings of others
(Pilger et al. 2010).
Many of the fish species in our stable isotope analysis demonstrated elevated carbon signatures relative
to the collector-filterer invertebrates used as a baseline, suggesting the contribution of an alternative
carbon source to the food web. As consumer carbon
stable isotope signatures are elevated relative to the
collector-filterers, it is likely that the additional
resources contributing to the food web are detritus
and invertebrates from slow-water habitats (Finlay
et al. 2002). An alternative basal resource could have
implications for our interpretation of trophic position
if the nitrogen signature of the primary consumers
demonstrating elevated d13C is different than the
signature demonstrated by the collector-filterers used
in our analysis. However, the results of a previous
desert stream study (Gido et al. 2006) suggest that
Effects of multiple invaders on imperiled desert fishes
algae and detritus have similar d15N signatures.
Previous studies have demonstrated that each of the
‘three species’ is omnivorous, consuming benthic
invertebrates, algae, detritus and in the case of roundtail chub, fish and terrestrial invertebrates (Childs
et al. 1998; Bezzerides & Bestgen 2002; Quist et al.
2006). Thus as collector-filterer insects dominated
our benthic invertebrate samples, we believe that the
use of collector-filterer insects as a baseline is sound.
We recognise there are potential limitations to our
inference of both the trophic structure and relative
growth rates between the upper and lower San Rafael
River. Previous research suggests using caution when
estimating annual growth from more than the single
most recent annuli, as this method inherits uncertainties due to size-selective mortality (i.e., Lee’s
phenomenon; Gutreuter 1987). However, by including all annuli in the analysis, we were able to
estimate growth in years when the populations were
not sampled, or when fin ray sections were not
collected. In addition, an analysis of body condition
revealed similar results to our size-at-age analysis
(Walsworth 2011). Isotopic signatures often vary
with fish length and growth rate, as well as over time
(Harvey et al. 2002; Vinson & Budy 2011), another
potential limitation of our data. However, ontogenetic
diet shifts, if present, would result in more conservative estimates of non-native piscivore trophic positions, as smaller individuals would not yet be
piscivorous. While the data collected for this study
cannot explicitly demonstrate predation, greater
competition or a change in fitness for the ‘three species’, the weight of evidence from our stable isotope
analysis, abundance comparisons (T.E. Walsworth &
P. Budy in review) and the results of previous studies
throughout the Colorado River Basin suggest that the
non-native fishes are having substantial impacts on
populations of the ‘three species’. These negative
impacts appear to result from the establishment of
novel predators and competitors in the ecosystem and
extensive restructuring of the aquatic community.
The reduction or loss of native species in an ecosystem can lead to overwhelming ecosystem level
effects, including, but not limited to, further species
loss or reduced ecosystem resilience (Wootton &
Downing 2003; Lockwood et al. 2007). Given the
high densities of non-native fishes in the lower river,
the lack of significant increase in native fish density
in complex habitat in the presence of non-native
fishes, and the associated impacts suggested herein,
restoration of physical habitat in the lower river may
have little effect on ‘three species’ populations in the
absence of efforts to minimise the effects of nonnative fish species (Walsworth 2011). Improving the
physical habitat template could actually enhance nonnative performance and abundance (Bond & Lake
2003). As such, the eradication of non-native fishes
may be a necessary step to ensure the persistence of
the ‘three species’ throughout their native range,
although the effectiveness of such a strategy may be
most effective in combination with restoration of a
more natural flow regime (Gido & Propst 2012). Our
results demonstrate that non-native fish species significantly alter the food web structure of the San
Rafael River, presenting novel predators and competitors that threaten the persistence of these endemic
and imperilled species. Maintaining connectivity with
‘three species’ populations in the upper San Rafael
River (while avoiding upstream expansion by nonnative species) and the main-stem Green River may
be critical to the persistence of the ‘three species’
in the lower river (Pulliam 1988; Bottcher 2009;
Walsworth 2011).
Acknowledgements
We would like to thank Charles Hawkins and Michelle Baker
for their thoughtful comments on previous drafts of this manuscript. B. Simcox, J. Remington, K. Wilson, S. Petre, D. Cole,
P. Nicholson, R. Chaston, D. Fowler, P. Tuttle, M. Schifiliti,
T. Wright, W. Gordon, J. Baker, D. Collins and D. Olsen
helped in the field and laboratory. This research was funded
by United States Bureau of Reclamation Activities to Avoid
Jeopardy Program, an S.E. and Jessie E. Quinney Fellowship,
and the Ecology Center at Utah State University. Additional
support was provided by the U.S. Geological Survey – Utah
Cooperative Fish and Wildlife Research Unit (in kind), the
U. S. Bureau of Land Management, and the Utah Division of
Wildlife Resources. Two anonymous reviewers provided constructive comments on previous drafts of this manuscript. The
use of trade names or products does not constitute endorsement by the United States Government. This study was performed under the auspices of Utah State University IACUC
protocol 1310.
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