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22001155 SOUTHEASTERN NATURALIST 1V4o(2l.) :1347,3 N–3o9. 62
Trophic Variation in Coastal Plain Stream Predatory Fishes
Dean E. Fletcher1,*, Angela H. Lindell1, Garrett K. Stillings1, Gary L. Mills1,
Susan A. Blas2, and J Vaun McArthur1
Abstract - Unique morphologies along with associated differences in habitat use and feeding
behavior can result in fish at the top of piscine food chains differing in trophic level.
Broad size ranges inherent within large species provide opportunity for size-related trophic
shifts. Such relationships between size and trophic level can be species specific. Furthermore,
individual-based diet variation can bring about differences among similar-sized
organisms. A challenge to aquatic ecologists is deciphering these patterns of trophic change
both between and within species. Stable isotope analysis has emerged as a powerful tool
for evaluating such patterns. Employing stable isotope analyses, we assessed trophic differentiation
in 4 large predatory fish species from a coastal-plain stream. We established the
trophic base by including 2 herbivorous invertebrates in the analysis and identified a trophic
hierarchy among species, with 2 specialized, generally open-water piscivores, Lepisosteus
osseus (Longnose Gar) and Micropterus salmoides (Largemouth Bass), occupying the highest
trophic position. The largest-bodied and generally benthic-oriented species, Ictalurus
punctatus (Channel Catfish), occupied the lowest trophic level among the fishes studied.
Trophic position of Largemouth Bass and Longnose Gar increased linearly and gradually
with size within the broad size ranges collected. In contrast, Channel Catfish exhibited a
more abrupt shift in trophic position with size and much individual variation associated with
the shift. Additionally, groups of Longnose Gar had belonged to distinctly different food
chains, despite coexisting in a relatively small stream when collected. Differences between
the observed patterns and other published accounts indicate further evaluation of trophic
patterns of these fishes among habitats is warranted.
Introduction
Trophic relationships involving predatory fishes have diverse and extensive influences
on stream ecosystems at multiple levels of organization. Presence of fish
predators has been shown to modify stream-community compositions (Bechara et
al. 1992, Jackson et al. 2001, Williams et al. 2003) by reducing both numbers and
feeding efficiency of stream herbivores and consequently influencing the processing
of stream basal-energy resources such as allochthonous detritus (McIntosh et
al. 2005, Ruetz et al. 2002) and attached algae (Bechara et al. 1992, Gelwick 2000,
Power 1990, Power et al. 1985). However, herbivore efficiency is not always affected
by fish predators (Ruetz et al. 2002). Other effects of predatory stream fishes
include habitat shifts of prey species (Englund and Krupa 2000; Power et al. 1985;
Schlosser 1987, 1988) and altered prey life histories (Peckarsky et al. 2002). The
presence of fish predators in mercury (Hg)-contaminated ponds influenced the Hg
Savannah River Ecology Laboratory, University of Georgia, PO Drawer E, Aiken, SC
29802. 2Area Completion Projects, Savannah River Nuclear Solutions, Savannah River Site,
Aiken, SC 29808. *Corresponding author - fletcher@srel.uga.edu.
Manuscript Editor: Morgan E. Raley
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pool present in the macroinvertebrate community and indirectly the risk to various
terrestrial predators of consuming contaminated prey (Henderson et al. 2012). Consequently,
understanding the trophic status of large fishes is essential to defining the
role the organisms may play in aquatic ecosystems.
The trophic level of stream fishes varies not only among species and feeding
guilds, but also among individuals within a species. This intraspecific variation is
particularly evident in large predatory fishes where broad size ranges of individuals
can concurrently reside in a stream. Ontogenetic or size-related trophic shifts can
be as important as taxonomic differences (sensu Woodward and Hildrew 2002). Juveniles
of piscivorous fish species feed on zooplankton or other small invertebrates
and as they grow switch to larger invertebrates or fish larvae before finally shifting to
larger fish prey as adults (Keast 1985, Mittelbach and Persson 1998). Within a species
or feeding guild, size of prey generally continues to increase with predator body size
(Keast 1985, Mittelbach and Persson 1998, Sheldon and Meffe 1993), allowing large
predators to consume prey sizes unavailable to relatively smaller predators (Wilson
1975). Thus, the range of prey sizes and number of species consumed often increases
with predator body size (Scharf et al. 2000), but prey availability can influence predator
diet and consequently trophic level in any particular system (Layman et al. 2005,
Wilson 1975). The pace of progression to piscivory may also be heavily influenced
by the level of specialization toward piscivory (Keast 1985). Consequently, the size
of large fish predators is not always an indicator of trophic status as a result of such
morphological or behavioral specializations. Much trophic divergence occurs at the
family or generic levels (Sheldon and Meffe 1993) due to morphological distinctions
being more pronounced at these levels. Large syntopic predators have partitioned
their habitats through evolutionary processes that have altered morphologies, including
size and form of their mouths and bodies as well as behaviors (Gatz 1979, Keast
and Webb 1966, Wikramanayake 1990, Winemiller 1989). These evolved characteristics
interact to influence the potential diets of these predators.
Classic diet studies examining fish gut contents provide a snapshot of what a fish
has recently eaten. These studies do not make inferences about nutrient assimilation
nor are they indicative of what the fish has eaten over a longer time period
(Bearhop et al. 2004, Gu et al. 1996, Vander Zanden and Vadeboncoeur 2002).
Additionally, diet studies often need to assume trophic interactions among lower
trophic levels such as small aquatic invertebrates (Vander Zanden et al. 1997).
Stable isotopes of nitrogen (N) and carbon (C) are becoming more commonly
incorporated into studies of trophic relationships as tools to understand the importance
of different basal resources and the trophic status among and within species.
Organismal tissue contains 2 stable isotopes of N: 14N and the heavier isotope 15N.
Comparison of the ratios of 15N to 14N (δ15N) is informative of trophic position, because
as N is transferred from one trophic level to another, tissue generally becomes
more enriched with the heavier isotope by ~3.4‰ (Post 2002). Consequently, a
higher δ15N is indicative of a higher trophic level.
Two stable isotopes of C are also present in organismal tissue: 12C and the
heavier isotope 13C. However, in contrast to N, the ratio of 12C and 13C (δ13C)
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generally changes less between trophic transfers, with enrichment of the heavier
isotope (13C) between trophic levels usually less than 1.6‰ (McCutchan et al.
2003). The δ13C provides information on the source of C acquired by an organism
in respect to the basal resources of a system. An advantage of stable isotope
analysis (SIA) is that assimilation of these isotopes into tissue results in an
analysis of ingested materials integrated over a longer time period than diet studies
(Vander Zanden and Vadeboncoeur 2002). Additionally, only assimilated
materials are analyzed, and all trophic transfers are assessed—even among invertebrates
(Vander Zanden and Vadeboncoeur 2002, Vander Zanden et al. 1997).
However it is often difficult to establish variability in stable isotope signature
shift between different organisms, spatial and temporal variability in signatures,
base autotroph signatures, and the effects of organism physiology and age, sample
preparation, and physical factors such as water velocity on signatures (Finlay
2004, Finlay et al. 1999, France 1996, McCutchan et al. 2003, Overman and Parrish
2001, Post 2002).
The versatility of SIA of C and N in ecological studies is evident in scientific
literature. Trophic arrangement of aquatic communities has been revealed in lentic
(Gu et al. 1996, Kupfer et al. 2006) and lotic systems (Jepsen and Winemiller
2002). Moreover size-related trophic shifts within a species have been shown (Gu
et al. 1996). Portions of diet items actually assimilated and diet variability has been
assessed (Atkinson et al. 2010, Raikow and Hamilton 2001). Distinctions between
the assimilation of terrestrial versus aquatic sources of primary production have
been made in lotic systems (Finlay 2001, Fuentes Brito et al. 2006, Zah et al. 2001)
as has the converse incorporation of C from in-stream primary production into terrestrial
food webs (Collier et al. 2002). Within a stream, SIA was used to determine
whether assimilated food was derived from local or upstream sources (Finlay et
al. 2002). SIA has also revealed the relative contributions of various primaryproduction
sources to lentic food webs (Hecky and Hesslein 1995, Herwig et al.
2004, Vander Zanden and Vadeboncoeur 2002). In stream-spawning Salmo trutta L.
(Brown Trout), SIA distinguished anadromous from freshwater-resident individuals
by differentiating the food webs of each (McCarthy and Waldron 2000). Some
types of pollution such as human sewage, barnyard runoff, or synthetic N fertilizers
can modify stable isotope signatures (e.g., increase δ15N; Cabana and Rasmussen
1996, Lake et al. 2001, Wayland and Hobson 2001), but SIA of C and N has been
used successfully in habitats contaminated by coal-combustion waste (Unrine et al.
2007) such as our study area. Despite the difficulties discussed earlier, SIA provides
a powerful tool for use in aquatic ecological studies.
Our objectives were to (1) compare the trophic position of 4 species of large
predatory fish in a coastal-plain stream, (2) compare the relationship between body
size and trophic position among these species, (3) investigate whether specific
changes in morphology such as gape or head width influenced the observed relationships
between body size and trophic positions, and (4) compare carbon sources
among the 4 species of predatory fish and also determine whether they shifted with
size or trophic level within a species.
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Field-Site Description
Beaver Dam Creek (BDC), a Savannah River tributary, is located on the Savannah
River Site (SRS) along the southeast border of South Carolina. The SRS is an
801-km2 National Environmental Research Park operated by the US Department
of Energy since 1951. Beaver Dam Creek has been impacted by a coal-fired electric-
and steam-generating power plant operated in its headwaters since the early
1950s (Halverson et al. 1997). A more complete study-site description is provided
in Fletcher et al. (2014a, b), but summarized here. Upper reaches of BDC were
channelized to carry large volumes of Savannah River water from the power house
along with effluents from associated ash- and coal-pile runof f basins.
Our study sites situated at the edge of the Savannah River floodplain and Aiken
Plateau supported species associated with large rivers as well as those typical of
smaller upland tributaries. Although many species were rare, we collected 46 species
of fish from this area. As part of a larger study, we established 2 sites in the upper
3.2 km of BDC separated by only 430 m, but differing substantially in hydrologic
regime. The upstream site A lies on fluvial terraces of the Savannah River and has
deeply incised, scoured channel with an inactive floodplain. The downstream site
B lies on the Savannah River floodplain with a less-incised channel and an active
floodplain that is inundated by both BDC and Savannah River water during floods.
Although patterns and processes in the downstream site are not all independent from
the upstream site, we sought to make comparisons based on unique hydrology and
geomorphology found at each site. Previously reported differences between these
sites include stable isotope signatures of invertebrates (Fletcher et al. 2014b).
Study Organisms
In our study stream, we found 4 species of large fishes: Lepisosteus osseus (L.)
(Longnose Gar), Ictalurus punctatus (Rafinesque) (Channel Catfish), Micropterus
salmoides (Lacépède) (Largemouth Bass), and Amia calva L. (Bowfin). These
native species each exceed 400 mm standard length (SL) as adults, are commonly
syntopic in southeastern US coastal plain streams, and vary greatly in head and
body forms. Size of these large predators precludes the largest adults of these species
from preying upon each other, but it is not visually apparent which species
occupy the highest trophic level.
Largemouth Bass have a robust fusiform body, a deep emarginate tail, a large
terminal mouth, and large eyes relative to their head and body size. These are characteristics
that well suit it to be a roving predator (Gatz 1979).
The anterior of a Channel Catfish is relatively ventrally flattened and its tail
has a deeply forked caudal fin, especially in smaller individuals. A conspicuous
feature of Channel Catfish is sensory barbels surrounding its mouth. As apparent
by their relatively small eyes and high number of sensory receptors on the
barbels and body of Channel Catfish (Caprio et al. 1993), catfishes rely less on vision
for capturing prey and more on tactile and chemical responses. Although its
subterminal mouth predisposes it to bottom feeding (Gatz 1979, Moyle and Cech
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1982, Wikramanayake 1990), Channel Catfish will feed at multiple water levels
(Eddy and Underhill 1974).
Longnose Gar have an elongate, round body, rounded caudal fin, and posteriorly
located dorsal fin characteristic of an ambush or stalking predator (Gatz 1979,
Keast and Webb 1966). Their head is highly specialized with narrowly elongate,
highly toothed jaws well-suited for capturing fish as prey (Netsch 1964, Marcy et
al. 2005). Like the Largemouth Bass, the Longnose Gar has large eyes relative to
their head size.
Bowfin have a long, moderately rounded body anteriorly but more compressed
posteriorly with a rounded caudal fin and elongate dorsal fin consistent with a lieand-
wait predator (Gatz 1979). Its mottled coloration helps camouflage it in the
highly vegetated waters that it typically inhabits (Marcy et al. 2005).
Since herbivores integrate sources of primary production feeding a stream (Cabana
and Rasmussen 1996,Vander Zanden et al. 1997), we included 2 herbivorous
invertebrates to establish isotopic signatures of the food-web base. Corbicula fluminea
(Müeller) (Asiatic Clam) filter-feeds particles from the water column and
deposit-feeds materials from surface sediments (Hakenkamp et al. 2001). The heptageniid
mayfly Maccafertium modestum (Banks) scrapes biofilm from the surface
of submerged objects such as wood debris or facultatively collects leaf particles
(Kondratieff and Voshell 1980, Merritt et al. 2008). A more complete description
of these species is provided in Fletcher et al. (2014b), which compares the trophic
levels and carbon sources between these 2 stream invertebrates.
Methods
Sample collection and tissue handling
We collected invertebrates from 14 January through 11 May 2010 using
dip nets or seines, and fish from 20 May through 28 July 2010 mostly
collected by boat-mounted electrofishing (collected on 16 days) but also with
supplemental sampling efforts using seines, minnow traps, hoop nets (trapped
on 20 days), and backpack electrofishers (collected on 5 days). All fish were
frozen and later thawed and rinsed first in tap water and then in 18-milliohm
(MΩ) deionized water prior to processing. We measured SL (mm), total length
(TL; mm), and total wet body mass (g), and removed a skinless subsample of
muscle from the right anterodorsolateral region of each fish for stable isotope
analysis. Tissue samples were lyophilized, ground to a fine powder, and homogenized
prior to analysis. We determined sex and maturity by gonadal inspection.
Because collection occurred during the late spring through mid-summer, gonads
of adult fish were generally not highly regressed. Consequently, the sex was
generally apparent; however, we confirmed the sex of the Longnose Gar gonads
according to Ferrara and Irwin (2001). We measured gape and head widths on
Channel Catfish and Largemouth Bass because these characters can influence size
of prey consumed (Gatz 1979, Keast and Webb 1966). Longnose Gar were excluded
from the head-feature analyses due to their unique head morphology, and
Bowfin were excluded because of small sample size.
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Laboratory handling of M. modestum and Asiatic Clams are detailed in Fletcher
et al. (2014b). We analyzed a total of 13 M. modestum composite samples (site
A: n = 5; site B: n = 8) and 19 Asiatic Clam composite samples (site A: n = 11;
site B: n = 8). We collected and analyzed a total of 5 Bowfin, 51 Channel Catfish,
34 Largemouth Bass, and 19 Longnose Gar (Table 1). Our sampling efforts were
focused on many species outside of the scope of this analysis. We attempted to collect
a range of sizes of each species, but some species were more difficult to collect
adequate sample sizes of than others. We released all Longnose Gar and Channel
Catfish after an adequate sample was attained, but needed to keep all captured Bowfin
and Largemouth Bass for analysis.
Stable isotope analyses
Stable isotope analyses of C and N were performed on a Finnigan Delta Plus
mass spectrometer (Thermo-Finnigan, Bremen, Germany) in the Stable Isotope and
Soil Biology Laboratory, Odum School of Ecology, University of Georgia. Isotope
ratios were expressed in the delta (δ) format:
δ 13C or δ15N (units of ‰) = ([Rsample - Rstandard] /Rstandard) x 1000,
where R is the 13C:12C ratio or 15N:14N ratio (Atkinson et al. 2010). A bovine standard
was referenced against an international standard (Atkinson et al. 2010), and
precision averaged ≤0.1%.
Statistical analyses
After assessing normality of our data, we improved the distribution of δ15N,
δ13C, SL, gape width, and wet body mass by loge transformation prior to analyses.
Additionally, we arcsine square-root transformed relative gape width (Zar 1984).
Using 2-sample t-tests, we compared the δ15N of Channel Catfish, Largemouth
Bass, and Longnose Gar between sexes and between adults versus juveniles.
Similar comparisons of δ13C for these species between sexes, size groups, and between
adults versus juveniles were made. We were unable to determine the sex of
1 juvenile Largemouth Bass, so we excluded it from analyses of sex. Using least
squares linear regression, we individually evaluated the relationships of δ15N and
gape width with total wet body mass and SL, as well as the relationship between
δ15N and gape width. We graphically assessed homoscedasticity of the regression
residuals. The graphs illustrating linear regression lines include the 95% confidence
intervals. We compared the δ15N and δ13C between sites and among species using
analysis of variance (ANOVA) models that included site, species, and the associated
interaction term and used Tukey pairwise comparisons to further evaluate
differences among species. The ANOVA models were repeated including only the
4 fish species to confirm the reliance of the significant interaction term on spatial
differences in the less-mobile invertebrates. Spatial variation of the invertebrates
has been previously addressed (Fletcher et al. 2014b).
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Results
Intraspecific trophic variation
We collected broad size ranges of Channel Catfish and Largemouth Bass that
spanned from small juveniles to large adults (Table 1). However, we did not
collect any Longnose Gar smaller than 444 mm SL or Bowfin smaller than 367
mm SL. Trophic position (δ15N) did not differ between sexes in Channel Catfish,
Largemouth Bass, or Longnose Gar (Table 2), and sample size precluded
Table 1. Species, sizes, and sex of fish included in the analyses. SL = standard length, F = female, M
= male, and U = unknown sex, A = adult, J = juvenile.
Species n SL (mm) Whole wet weight (g) Maturity (n)
Bowfin (A. calva)
Females 1 506 2012 1 A, 0 J
Males 4 423 (367–465) 1200 (765–1551) 4 A, 0 J
Channel Catfish (I. punctatus)
Females 28 410 (240–563) 1515 (224–3497) 23 A, 5 J
Males 23 382 (99–700) 1623 (16–6870) 9 A, 14 J
Largemouth Bass (M. salmoides)
Females 21 214 (97–480) 385 (16–2250) 9 A, 12 J
Males 12 179 (97–317) 187 (16–736) 4 A, 8 J
Unknown sex 1
Longnose Gar (L. osseus)
Females 7 801 (612–962) 2255 (825–3913) 7 A, 0 J
Males 12 527 (444–645) 529 (261–1084) 12 A, 0 J
Table 2. Comparison of the average δ15N and δ13C between males and females, and adults and
juveniles for each of our study species. Mean ± standard deviation with the limits in parentheses. Associated
P values for 2-sample t-tests are provided.
Males Females P Adults Juveniles P
δ15N (‰)
Longnose Gar 13.9 ±0.8 14.6 ± 1.4 0.30 14.2 ± 1.0 - -
(12.7–15.1) (11.8–15.7) (11.8–15.7) -
Largemouth Bass 13.1 ±0.7 13.6 ± 1.2 0.15 14.1 ± 1.3 13.0 ±0.6 0.01
(12.0–14.1) (12.0–17.6) (12.6–17.6) (12.0–14.2)
Channel Catfish 11.4 ±0.8 10.9 ± 1.1 0.63 11.1 ± 1.1 11.2 ±0.7 0.44
(10.1–12.9) (8.8–13.7) (8.8–13.7) (10.1–12.8)
Bowfin 13.0 ±1.5 11.4 - 12.7 ± 1.5 - -
(11.1–14.7) - (11.1–14.7) -
δ13 C (‰)
Longnose Gar -23.9 ± 3.2 -22.7 ± 3.2 0.39 -23.4 ± 3.2 - -
(-26.6 to -15.9) (-25.8 to -17.9) (-26.6 to -15.9) -
Largemouth Bass -25.6 ± 0.5 -25.7 ± 0.8 0.61 -25.7 ± 1.0 -25.7 ±0.4 0.81
(-26.6 to -24.8) (-28.4 to -24.6) (-28.4 to -24.6) (-26.9 to -25.2)
Channel Catfish -26.1 ± 1.1 -26.0 ± 1.1 0.92 -26.1 ± 1.3 -26.0 ±0.5 0.38
(-29.0 to -23.3) (-27.8 to -23.6) (-29.0 to -23.3) (-26.9 to -25.2)
Bowfin -27.3 ± 1.2 -28.3 - -27.5 ± 1.1 - -
(-28.8 to -26.0) - (-28.8 to -26.0) -
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comparison within Bowfin. However, with the wide range of fish sizes within
each species, size-related trophic shifts were noted.
The δ15N of Longnose Gar spanned a narrow range: 3.9‰ (11.8–15.7, SD = 1.0).
A weak linear relationship occurred between δ15N and both body mass (R2 = 0.17,
β = 0.03, P = 0.08; Fig. 1a) and SL (R2 = 0.18, β = 0.12; P = 0.07) of that species.
The δ15N of Largemouth Bass spanned the broadest range of the 4 species: 5.6‰
(12.0–17.6, SD = 1.1‰). However, 32 of 34 Largemouth Bass ranged only 2.2‰
(12.0–14.2). The δ15N was higher in adult than juvenile Largemouth Bass (Table 2),
but this could be driven by body size. Across all sizes of Largemouth Bass, the relationship
between body size and δ15N was a simple linear relationship indicating a
gradual increase of trophic position with increasing body mass (R2 = 0.31, β = 0.02,
P < 0.01; Fig. 1b) and SL (R2 = 0.30, β = 0.08, P < 0.01). Additionally gape width
increased with body mass (R2 = 0.99, β = 0.33, P < 0.01; Fig. 2a) and SL (R2 = 0.99,
β = 1.06, P < 0.01). Consequently the Largemouth Bass δ15N and gape width were
also linearly related (R2 = 0.29, β = 0.07, P < 0.01; Fig. 2c). Although allometric
growth in Largemouth Bass does result in relative gape width (as a proportion of
SL) being greater (P < 0.01) in adults (mean = 9.4 %, SD = 0.40) than juveniles
Figure 1. Relationship of δ15N and whole wet body mass for (a) Longnose Gar, (b) Largemouth
Bass, (c) Channel Catfish with gape width of <34 mm, and (d) Channel Catfish with
gape width of >34 mm. Regression lines and 95% confidence interv als are illustrated.
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(mean = 8.3 %, SD = 0.55), the difference is not great. Across all sizes of Largemouth
Bass, gape width ranged 38.4 mm (7.5–45.9), but relative gape width was
only 2.6% SL (7.5–10.1).
For both Largemouth Bass and Longnose Gar there was 1 fish that was aberrant
from the rest. These outliers were particularly evident in the linear-regression
residuals. Since we were unable to rerun tissue samples from these 2 fish, it is not
known if the observed values are handling mistakes or curious observations. For
Largemouth Bass, removal of the putative outlier increases the amount of variation
explained by linear regression of δ15N and whole body mass (R2 = 0.41, β =
0.02, P < 0.01). Similarly for Longnose Gar, exclusion of the single outlier results
in a more highly significant linear relationship between δ15N and whole body mass
(R2 = 0.35, β = 0.04, P = 0.01). The δ15N of Bowfin spanned 3.6‰ (11.1–14.7, SD =
1.5), but collection of only 5 individuals precluded examination of the relationship
between body mass and δ15N for the Bowfin.
Figure 2. Relationship of gape width and whole wet body mass for (a) Largemouth Bass
and (b) Channel Catfish. Relationship δ15N and gape width for (c) Largemouth Bass and (d)
Channel Catfish (open circles = Channel Catfish with gape width of <34 mm; closed circles
= Channel Catfish with gape width of >34 mm). Regression lines and 95% confidence intervals
are illustrated.
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The δ15N of Channel Catfish ranged 4.8‰ (8.8–13.7, SD = 1.0). Across all
sizes of individuals, the δ15N of Channel Catfish was not linearly related to body
mass (R2 < 0.01, β = 0.00, P = 0.64) or SL (R2 = 0.01, β = 0.02, P = 0.61). The
δ15N also did not differ between adults and juveniles (Table 2). Across all sizes of
Channel Catfish, gape width ranged 87.2 mm (11.2–98.4), which corresponds to
a range in relative gape width (% SL) of 7.2 (8.2–15.5). Gape width linearly increased
with body mass (R2 = 0.93, β = 0.40, P < 0.01; Fig. 2b) and SL (R2 = 0.93,
β = 1.24, P < 0.01). However, the δ15N was also not linearly related to gape width
(R2 = 0.03, β = 0.03, P = 0.25). Further investigation revealed a more complex relationship.
The relationship between gape width and δ15N changed at a gape width
of around 34 mm. When less than 34 mm, gape width ranged 20.3 mm and relative
gape width ranged 4.1% SL. When greater than 34 mm, gape width ranged 63.4
mm and relative gape width ranged 6.1% SL. When gape width was less than 34
mm, the δ15N decreased with gape width (R2 = 0.32, β = -0.10, P < 0.05; Fig. 2d)
and body mass (R2 = 0.38, β = -0.03, P < 0.03; Fig. 1c). In contrast, δ15N increased
with gape width (R2 = 0.28, β = 0.17, P < 0.01; Fig. 2d) and body mass (R2 = 0.24,
β = 0.08, P < 0.01; Fig. 1d) when gape width exceeded 34 mm.
Community trophic hierarchies
The δ15N differed among species, with the 2 herbivorous invertebrates occupying
the lowest trophic position, Channel Catfish intermediate, and Bowfin, Largemouth
Bass and Longnose Gar the highest (ANOVA: R2 = 0.90, species P < 0.01, site P =
0.01, species*site P <0.01, pairwise comparisons P < 0.05; Fig. 3a). On average,
Channel Catfish is at a lower trophic position than the other fishes. However, with
the wide range of δ15N and associated size-related shifts occurring in Channel Catfish,
some larger individuals begin to overlap with that of smaller individuals of
both Largemouth Bass and Longnose Gar (Figs. 3, 4). The latter 2 species broadly
overlap in trophic position. The position of Bowfin is less certain due to relatively
high variability among the small sample size.
Pairwise comparisons indicated the significant site and species*site interaction
term was driven by spatial variability in the δ15N of M. modestum (pairwise comparison
P < 0.01). In contrast, the δ15N of the other species did not differ between
sites (pairwise comparisons P > 0.90). Correspondingly, the same ANOVA model
including only the fish indicated differences between species, but not sites (R2 =
0.63, species P < 0.01, site P = 0.99, species*site P = 0.40). Interestingly, with all
fish species included, δ15N was negatively correlated to body mass (rranks = -0.203,
P < 0.05) and not correlated to body length (rranks = -0.082, P > 0.10). However,
Figure 4 clearly shows these relationships were driven by the Channel Catfish occupying
a lower trophic level despite its heavy body.
Carbon sources
The δ13C of Largemouth Bass, Bowfin, and Channel Catfish spanned 3.8‰ (-28.4
to -24.6, SD = 0.7), 2.9‰ (-28.8 to -26.0, SD = 1.1), and 5.7‰ (-29.0 to -23.3, SD
= 1.1), respectively. Whether comparing size groups established from size frequencies
or adults versus juveniles (Channel Catfish: 16–1612 g and 1936–6870 g,
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Figure 3. Mean δ15N and δ13C of C. fluminea (Asiatic Clam), M. modestum, A. calva (Bowfin),
I. punctatus (Channel Catfish), M. salmoides (Largemouth Bass), and L. osseus (Longnose
Gar) represented by black circles. Error bars represent + 1 standard error. Gray lines
represent measures of individuals.
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respectively; Largemouth Bass: 14–180 g and 264–2250 g, respectively; Longnose
Gar: 261–1145 g and 1644–3913 g, respectively), δ13C was not dependent upon size
(all P > 0.35; Table 2). Similarly, the δ13C also did not differ between sexes of Channel
Catfish, Largemouth Bass, or Longnose Gar (all P > 0.38; Table 2). Spanning
a range of 10.66‰, the δ13C of Longnose Gar was substantially more variable than
the other 3 species. Additionally, 2 groups could be identified in the Longnose Gar
population, with the δ13C of 1 group averaging -19.29‰ (n = 6, SD = 2.16, range
= -21.72 to -15.93) and the other averaging -25.34‰ (n = 13, SD = 0.66, range =
-26.59 to -24.47). We were unable to contribute this δ13C distribution to size, sex,
site, or trophic position.
Carbon sources based on δ13C statistically differed between groups of species.
The δ13C was lowest and similar among Asiatic Clam, M. modestum, and Bowfin,
intermediate and similar in Channel Catfish and Largemouth Bass, and on average
highest in Longnose Gar (R2 = 0.71, species P < 0.01, site P < 0.01, species*site
P < 0.01; pairwise comparisons P < 0.05; Fig. 3b). However, the average falls in between
the 2 groups of Longnose Gar. Consequently, only Longnose Gar individuals
of the more enriched δ13C group do not overlap with any of the other species. The
mean δ13C of Bowfin appears only marginally lower than Channel Catfish (pairwise
comparison P = 0.06). Again, the significant site and interaction term was driven by
spatial variability in the invertebrates, and fish did not significantly differ between
sites (pairwise comparison P > 0.77). The same ANOVA model including only the
fish also indicated differences between species, but not sites (R2 = 0.35, species P <
0.01, site P = 0.23, species*site P = 0.32).
Figure 4. Species comparison of the relationship of δ 15N and body mass.
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Discussion
Trophic position calculations
A mean trophic fractionation or enrichment rate of 15N by 3.4‰ has been reported
from diverse habitats including aquatic and terrestrial systems, laboratory
and field studies, and organisms ranging from copepods to polar bears (Post 2002).
However, Post (2002) elaborated that an enrichment range from about 2 to 5‰ may
occur for any given trophic transfer. Similarly, a 3.3‰ enrichment of 15N between
trophic levels was calculated in a hypereutrophic subtropical lake (Gu et al. 1996)
and 2.8‰ in tropical streams (Jepsen and Winemiller 2002). Using laboratory
studies and literature, McCutchan et al. (2003) reported an average enrichment of
2.3‰, but indicated enrichment varies among organisms and stressed the uncertainty
inherent with this variability. Because of spatial, temporal, and taxonomic
variability, as well as anthropogenic influences, establishing an isotopic signature
representative of basal primary producers can also be notoriously difficult (Anderson
and Cabana 2007, Cabana and Rasmussen 1996, Jardine et al. 2006, Post 2002).
Long-lived herbivores such as freshwater mussels have been used as integrators
of primary production to convert the δ 15N to a trophic position using the equation
Trophic position = ([Predator δ15N–Herbivore δ15N]/3.4) + C,
where C equals the position of the organisms used to calibrate trophic position
(Cabana and Rasmussen 1996, Overman and Parrish 2001, Post et al. 2000,
Vander Zanden 1997). In a broad comparison of 5 invertebrate functional-feeding
groups in streams, scrapers have also been recommended for use in establishing a
trophic baseline (Anderson and Cabana 2007). Freshwater mussels are very rare
in the BDC system, so we used the average δ15N of our 2 herbivores, the scraper
M. modestum and deposit/filter feeding Asiatic Clam (trophic position = 2 ), to
estimate trophic position of the fishes. This may not be as optimal as larger and
longer-lived mussels, but because filter feeding, deposit feeding, and scraping biofilm
are included in these 2 species, many of the primary stream-energy sources are
represented. We calculated average trophic positions of 3.04, 3.50, 3.72, and 3.94
for Channel Catfish, Bowfin, Largemouth Bass, and Longnose Gar, respectively.
However future work should substantiate the enrichment rate in these organisms,
as we acknowledge the uncertainties inherent in using stable isotope signatures.
Because of their widespread distributions in coastal-plain streams, further evaluation
of using M. modestum and Asiatic Clam to establish a baseline for SIA food
web studies are warranted.
Interspecific trophic variation
Based on review of diet-survey literature, Roach et al. (2009) classified Longnose
Gar, Largemouth Bass, and Bowfin from the upper Mississippi River in
Minnesota as piscivores and Channel Catfish as an omnivore/detritivore. Subsequent
employment of SIA in the same study indicated a trophic hierarchy with
Longnose Gar > Largemouth Bass > Bowfin > Channel Catfish based on average
trophic positions of 4.25 > 3.98 > 3.78 > 3.62.. A similar hierarchy occurred among
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these same 4 species in BDC, despite all 4 species being at lower trophic positions
of 3.94, 3.72, 3.50, and 3.04, respectively. Since longer food chains lead to higher
trophic positions and food-chain length may increase with ecosystem size (Post et
al. 2000), it is not surprising that fish inhabiting a small stream such as BDC were
at lower trophic positions than the same species from a large system like the main
stem and backwaters of the Mississippi River.
A similar pattern to BDC was also observed in both forested and open canopy
habitats within a Texas reservoir with Lepisosteus oculatus Winchell (Spotted
Gar), Largemouth Bass, and Channel Catfish ranked 4.5 > 4.1 > 3.3 in forested
areas and 4.4 > 4.2 > 3.5 in open water, respectively (Chumchal and Hambright
2009). Similarly, trophic ranks were Lepisosteus platyrhincus DeKay (Florida Gar)
> Largemouth Bass > Bowfin in near shore habitats of a Florida lake, but were
Bowfin > Florida Gar > Largemouth Bass in marsh habitats of the lake inhabited by
smaller Largemouth Bass and more Bowfin (Fry et al. 1999). Other SIA studies of
freshwater ecosystems have placed gar species at the top of food webs dominated
by fishes. Florida Gar held the highest trophic position in another Florida lake (Gu
et al. 1996). Lepisosteus platostomus Rafinesque (Shortnose Gar) had the most
enriched δ15N of fishes in backwater lakes of the Mississippi and Illinois Rivers, IL
(Herwig et al. 2004, 2007). Even though the Florida Gar and Shortnose Gar reach a
smaller maximum size and have less-elongate jaws compared to the Longnose Gar,
the specialized morphology suited for piscivory often places gars at or near the top
of piscine food chains. This ranking is consistent with lower trophic specialization
at the species level (Keast 1985, Sheldon and Mef fe 1993).
Largemouth Bass also held the second highest trophic level in a Florida lake
(Gu et al. 1996). Literature and our study support Channel Catfish often inhabiting
a lower trophic position than equal-sized Bowfin, Largemouth Bass, and Gar. The
negative correlation between body mass and δ15N when all 4 BDC species were
combined resulted from the heaviest-bodied fish, Channel Catfish, occupying the
lowest trophic level. A general average trophic hierarchy of Longnose Gar (or other
gar species) > Largemouth Bass > Bowfin > Channel Catfish is consistent with our
data and published literature, acknowledging lack of statistical significance in some
of our comparisons and lack of statistical testing in some other studies. However,
location-specific habitat or community composition has the potential to favor individual
species.
Interspecific carbon source variation
δ 13C statistically differed among species, but generally followed the same pattern
as trophic level. The difference among species generally falls within the range that
would occur with an enrichment rate of around 1.6‰ per trophic transfer as reported
by McCutchan et al. (2003). Consequently basal C resources appeared to broadly
overlap among the 4 predatory fishes. This overlap of basal carbon sources by these
predators that integrate lower trophic levels into their diet was not surprising in a relatively
small stream. However, a portion of the Longnose Gars with entirely unique
carbon signatures was surprising and will be described in detail below.
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Intraspecific trophic variation
Specific patterns of trophic change are less established than the above-described
trophic hierarchies. However, general relationships between body size and diet or
trophic level have been widely studied. For example, size of eaten prey often increases
with predator size (Mittelbach and Persson 1998, Sheldon and Meffe 1993).
Such relationships between predator and prey size can arise from gape limitation
for predators that swallow their prey whole, thereby necessitating growth to a point
where large prey can be consumed (Winemiller 1989). Correspondingly, transitions
from eating invertebrates to a diet of fish can be size related and the portion of fish
found in a facultative piscivore’s diet increases with predator body size (Winemiller
1989). Two patterns in the relationship between trophic level and body size were
apparent in our study. Trophic position increased linearly within the collected size
ranges of both Longnose Gar and Largemouth Bass. Any abrupt change from lower
to observed trophic positions occurred at sizes smaller than those in our samples.
The smallest Longnose Gar and Largemouth Bass were 444 and 97 mm SL, respectively.
These patterns were also characterized by relatively low trophic variability
within size ranges (Fig. 1). In contrast, Channel Catfish exhibited a more abrupt
trophic shift.
Morphological specialization for piscivory can reduce the size and age at which
a species becomes piscivorous (Keast 1985). Moreover such specialization can reduce
a species’ ability to eat other prey types (Winemiller 1989), which will further
reduce trophic variability. Longnose Gars are a particularly specialized piscivore
with long, beak-like jaws for capturing prey by biting. Prey is swallowed whole
after capture. Diet studies have indicated that Longnose Gar can become largely
piscivorous at less than 100 mm TL, and adults have a diet of almost exclusively fish (Lagler
and Hubbs 1940, Mittelbach and Persson 1998, Netsch 1964). Fast growth can
also enable species to become piscivorous at younger ages (Mittelbach and Persson
1998). In addition to specialization, Longnose Gar is a fast-growing species that
can reach lengths of 400 mm TL in 1 year (Netsch and Witt 1962). Similarly, captive
Longnose Gar grew to 335 mm TL in 183 days in Florida and to an average of
290 mm TL in 267–325 days in Missouri (Carlander 1969). Our smallest Longnose
Gar was over 500 mm TL; thus all specimens captured likely had transitioned to
piscivory. Despite ranging from 444 to 962 mm SL, with the 1 outlier excluded, our
Longnose Gar spanned a range of only 0.87 trophic positions (3.51–4.38), with low
variability among similar-sized individuals. We suspect the observed variability in
trophic level in Longnose Gar that did occur stems from preying on fish of different
trophic positions.
Largemouth Bass are a large-mouthed suction feeder well suited for piscivory
(Keast and Webb 1966, Mittelbach and Persson 1998). Based on diet analysis and
SIA, Largemouth Bass young of the year (YOY) became piscivorous at 85 mm TL
in a small Michigan lake (Post 2003). Another study in Michigan lakes found 60%
of the YOY bass to be piscivorous at sizes over 40–50 mm SL (Olson 1996). In a survey
of diet studies, Mittelbach and Persson (1998) also indicated that Largemouth
Bass may begin to become piscivorous at a size less than 100 mm TL. Our smallest
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collected individuals exceeded these sizes. Positive relationships among gape size,
body size, and δ15N were observed in Largemouth Bass. Largemouth Bass trophic
level (range = 1.67 [3.28–4.95]) varied across a broader span than Longnose Gar, but
the increase was still relatively gradual. Thus again, any abrupt trophic shift occurred
at a size below our smallest individuals of 97 mm SL (16 g). Our largest Largemouth
Bass weighed 2.25 kg, twice that of our next largest bass. This largest individual occupied
a trophic position of 4.49 compared to 3.75 for the next largest individual and
the species average of 3.72. The trophic position of this single large individual fell
near the regression line between trophic position and body size, suggesting a continuous
and gradual increase in trophic level with size (Fig. 1b).
Habitat-related trophic shifts were noted in Largemouth Bass in a Florida lake,
with trophic position gradually increasing with body size (Fry et al. 1999). The δ15N
of Largemouth Bass also appeared to increase gradually with body size at locations
in the Colorado River system, CO (Martinez et al. 2001). In Rhode Island ponds and
small lakes, the δ15N of predators such as Largemouth Bass were less variable than
those of benthic-feeding fishes (Lake et al. 2001). Although relatively uncommon
in a hypereutrophic Florida lake, the δ15N of Largemouth Bass appeared to increase
more abruptly with size (Gu et al. 1996) in contrast to the gradual increase we found
in BDC. Consequently, variability among habitats and locations in the relationship
between trophic level and size should be the focus of further investigation.
Largemouth Bass can have a diverse diet including aquatic insects, crustaceans,
and fish (Marcy et al. 2005, Wiltz 1993). However in BDC, the broad overlap of the
Largemouth Bass δ15N with the extremely specialized Longnose Gar also suggests
piscivory in Largemouth Bass within most individuals.
In contrast, Channel Catfish exhibited more substantial trophic shifts in large individuals.
The shift began at gape widths exceeding 34 mm, with substantially more
individual variation in trophic level at the beginning of the shift (i.e., individuals
with gape widths just greater than 34 mm). Abrupt trophic changes can occur as
fish reach size thresholds that allow changes in feeding habits. For example, Cheilodactylus
spectabilis Hutton (Red Moki) off the coast of New Zealand exhibited
an abrupt diet shift thought to arise from an increased feeding suctorial force resulting
from larger body size (McCormick 1998). A similar abrupt trophic shift is
suggested by the relationship of size and trophic position in BDC Channel Catfish.
Allometric growth of body dimensions such as head and gape width resulted in
trophic level increasing with size in larger individuals. Subsequently, the largest
Channel Catfish adults began to overlap in trophic level with smaller Largemouth
Bass. In Lake Texoma, size-related diet shifts occurred in Channel Catfish, with
piscivory increasing in larger individuals (Edds et al. 2002). In that population, the
diet shift occurred at about 300 mm SL. Though trophic level increased with body
size, an abrupt trophic shift was not apparent in Channel Catfish in a Florida lake
(Fry et al. 1999); however, all Channel Catfish in that study were less than 800 g.
Channel Catfish from BDC with a gape greater than 34 mm ranged from 719 to
6870 g. We observed a trophic shift at a 34-mm gape width in our study stream, but
acknowledge that prey availability can influence such shifts in a location-specific
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manner (Winemiller 1989). Channel Catfish in the Savannah River had a diverse
diet of fish, aquatic insects, and crustaceans as observed through gut analyses
(Wiltz 1993).
Bowfin are voracious opportunistic predators with a diet of primarily fish and
crayfish (Lagler and Applegate 1942, Lagler and Hubbs 1940, Reighard 1903).
Bowfin trophic position increased with size in a Florida lake (Fry et al. 1999). The
δ15N of Bowfin from BDC ranged an equivalent of 1 trophic level (3.0–4.1), but
small sample size precluded thorough analyses of intraspecific variation. As expected,
neither the δ15N nor δ13C of any of the large, mobile predators differed between
sites. As described above, Longnose Gar (Johnson and Noltie 1996, McGrath et
al. 2012, Snedden et al. 1999), Largemouth Bass (Paller et al. 2005), and Channel
Catfish (Humphries 1965, Wendel and Kelsch 1999) regularly move further than the
430 m separating these sites.
Intraspecific carbon source variation
Movement of animals between food webs or ecosystems can result in individuals
possessing unique stable isotope signatures that appear as outliers in data
(Jardine et al. 2006). Accordingly, SIA has been employed to identify migrants into
a river from foreign food webs (Martinez et al. 2001, McCarthy and Waldron 2000).
Longnose Gar were unique among the 4 predators in having 2 distinct groups of
individuals based on carbon resources as indicated by δ13C. Interestingly, the δ13C
of the more 13C-enriched group of Longnose Gar does not overlap with any of the
other 5 species in this analysis. Moreover, they do not overlap that of 8 genera of
odonate (Dragonfly) nymphs or 3 species of Ameiurus (Bullhead Catfishes) analyzed
from this system during the same time period (D.E. Fletcher, unpubl. data).
Additionally, we could not find evidence of size, sex, reproductive condition, or site
contributing to this difference. Either the 2 unique groups of Longnose Gar were
part of 2 distinct food chains within BDC, which seems unlikely particularly given
the apparent uniqueness of the δ13C, or a portion of the population had recently immigrated
into that part of BDC.
Longnose Gar are known to be residents of mid-size streams such as BDC (Marcy
et al. 2005), but are also known to migrate from larger rivers into tributary streams
during spawning runs in the spring (Johnson and Noltie 1996, McGrath et al. 2012).
Documented migration distances of Longnose Gar have ranged from 10 to over 50
km (Johnson and Noltie 1996, McGrath et al. 2012), which exceed the total channel
length of BDC and supports the notion that migration is contributing to our observed
δ13C patterns. Following a spawning migration, Longnose Gar may remain in the
stream as long as 3 months before dispersing. Our collection times would have fallen
within the period when migrants may reside in the stream. Additionally, inundation
of the floodplain of large river systems can stimulate movements of several kilometers
(Snedden et al. 1999), and systems with large floodplains can result in seasonal
increases in niche breadth of riverine species (Jepsen and Winemiller 2002). The
Savannah River floodplain had been inundated the winter and early spring before
our fish collections. The importance of identifying these distinct groups of Longnose
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Gar in BDC was illustrated by Fletcher et al. (2014a), who found the group with the
unique δ13C had accumulated an order of magnitude higher concentrations of arsenic
in addition to other higher contaminant concentrations. Channel Catfish (Humphries
1965) and Largemouth Bass (Paller et al. 2005) are also often seasonally migratory,
but we did not observe distinct groupings based on 13C in these fishes. Either the
Channel Catfish and Largemouth Bass collected in BDC all had similar movement
patterns or the populations shared the same carbon source.
Conclusions
Though SIA signatures are known to exhibit extensive spatial variation (Guzzo et
al. 2011), a pattern we have observed for less-mobile organisms in the BDC system
(Fletcher et al. 2014b), the signatures of these highly mobile fishes did not differ
between sites. Overall, stable isotope analyses identified a trophic hierarchy among
species, with 2 specialized piscivores—Longnose Gar and Largemouth Bass—occupying
the highest trophic position. The largest bodied and more benthic-oriented
species, Channel Catfish, occupied the lowest trophic level. The trophic level of
Bowfin remains less clear due to our small sample size.
Largemouth Bass exhibited greater trophic variation than Longnose Gar, but
trophic level in both species increased in a gradual linear pattern across the broad
size ranges analyzed. Even though our Largemouth Bass ranged over a 160-fold
difference in body mass, trophic level increased gradually with body size as did
Longnose Gar, which exhibited a 15-fold body mass range. If any abrupt trophic
shifts occurred in these 2 species, the shifts occurred at sizes smaller than we analyzed.
Trophic variation among similar-sized individuals was relatively low, but
appeared to be highest in the smallest individuals. In contrast, Channel Catfish
showed a more abrupt trophic shift associated with greater individual variation,
particularly in the size ranges near where the shift started. Trophic position increased
with gape width in large individuals.
The importance of such trophic shifts is illustrated in Channel Catfish, for which
mercury concentrations of human health concern were found in the muscle only of
individuals that had begun the trophic shift (Fletcher et al. 2014a). The δ13C analysis
identified 2 groups of Longnose Gar, suggesting membership in different food
chains. Stable isotope analyses hold much potential in studying spatial foraging
patterns (Jepsen and Winemiller 2002) and the role of fish migrations in connecting
geographically separate food webs in coastal-plain streams. Future studies should
investigate the underlying causes of the observed variation among and within these
species. As many streams in the Southeast’s upper coastal plain have been extensively
impacted by anthropogenic stressors (EPA Report 2013), understanding
trophic relationships is an essential component to be incorporated into assessments
related to stream disturbance, preservation, restoration, or recovery in the region.
Acknowledgments
Funding was provided by the Area Completion Projects-SRNS. This work was also
supported by the Department of Energy under Award Number DE-FC09-07SR22506 to the
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University of Georgia Research Foundation. We thank Gary Meffe for insightful comments
that improved this manuscript and David Kling, Cynthia Tant, Beryl Walker, and Chandler
Tuckfield for field and lab assistance, and Tom Maddox for SIA.
Disclaimer: This report was prepared as an account of work sponsored by an agency of
the United States Government. Neither the United States Government nor any agency
thereof, nor any of their employees, makes any warranty, express or implied, or assumes any
legal liability or responsibility for the accuracy, completeness, or usefulness of any information,
apparatus, product, or process disclosed, or represents that its use would not infringe
privately owned rights. Reference herein to any specific commercial product, process, or
service by trade name, trademark, manufacturer, or otherwise does not necessarily constitute
or imply its endorsement, recommendation, or favoring by the United States Government or
any agency thereof. The views and opinions of authors expressed herein do not necessarily
state or reflect those of the United States Government or any agency thereof.
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