Download Disturbance and trajectory of change in a stream fish community

Oecologia
DOI 10.1007/s00442-013-2646-3
COMMUNITY ECOLOGY - ORIGINAL RESEARCH
Disturbance and trajectory of change in a stream fish community
over four decades
William J. Matthews • Edie Marsh-Matthews
Robert C. Cashner • Frances Gelwick
•
Received: 24 April 2012 / Accepted: 15 March 2013
Ó Springer-Verlag Berlin Heidelberg 2013
Abstract Communities can change gradually or abruptly,
and directionally (to an alternate state) or non-directionally.
We briefly review the history of theoretical and empirical
perspectives on community change, and propose a new
framework for viewing temporal trajectories of communities
in multivariate space. We used a stream fish dataset spanning
40 years (1969–2008) in southern Oklahoma, USA,
emphasizing our own 1981–2008 collections which included
well-documented, extreme drought and flood events, to
assess dynamics of and environmental factors affecting the
fish community. We evaluated the trajectory of the Brier
Creek community in multivariate space relative to trajectories in 27 published studies, and for Brier Creek fish, tested
Communicated by Jeff Shima.
Electronic supplementary material The online version of this
article (doi:10.1007/s00442-013-2646-3) contains supplementary
material, which is available to authorized users.
W. J. Matthews (&) E. Marsh-Matthews
Department of Biology, University of Oklahoma,
Norman, OK 73019, USA
e-mail: [email protected]
E. Marsh-Matthews
Sam Noble Oklahoma Museum of Natural History,
Norman, OK 73072, USA
R. C. Cashner
University of New Orleans, New Orleans, LA 70148, USA
Present Address:
R. C. Cashner
105 Continental Drive, Flat Rock, NC 28731, USA
F. Gelwick
Department of Wildlife and Fisheries Sciences, Texas A&M
University, College Station, TX 77843-2258, USA
hypotheses about gradual versus event-driven changes and
persistence of shifts to alternate states. Most species were
persistent, qualitatively, across the four decades, but varied
widely in abundance, with some having unusually strong
reproduction after extreme droughts. The community had an
early period of relatively gradual and directional change, but
greater displacement than predicted at random after two
consecutive extreme droughts midway through the study
(1998 and 2000). But, the community subsequently returned
toward its former state in the last decade. This fish community is characterized by species that are tolerant of environmental extremes, and have life history traits that facilitate
population recovery. The community appears ‘‘loosely stable’’ about a long-term average condition, but the impacts of
the two consecutive droughts were substantial, and may
foretell future dynamics of this or other communities in a
changed global climate if disturbance events become more
frequent or severe.
Keywords Drought Flood Long-term change Oklahoma Succession vectors
Introduction
‘‘How do communities change over time?’’ and ‘‘how do
communities respond to disturbances?’’ are two of the
long-standing, overarching questions in ecology, dating at
least to Shelford (1911). The theoretical approaches that
appeared in the middle of the last century (MacArthur
1955, 1960; Lewontin 1969; May 1973) for dynamics of
communities in n-dimensional space provided a framework
in which ecologists continue to view community dynamics.
Holling (1973) emphasized the role of random events, the
ability of a system to absorb perturbations or return to a
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Oecologia
previous state after disturbance, and the possibility for
community change by ‘‘sudden steps.’’ Using long-term
data for marine fouling communities, Sutherland (1974)
emphasized responses to perturbations and recognized
multiple stable points. Aggregating previous suggestions,
Connell and Sousa (1983) defined community stability both
quantitatively as ‘‘resistance’’ to change or ‘‘elasticity’’
after disturbance, and qualitatively as ‘‘persistence’’ of
species in a community. More recently, based on long-term
studies of prairie plant and animal communities, Collins
(2000) contributed the concept that real-world communities may exist over time in a global, ‘‘loosely stable’’
equilibrium.
Beginning in the 1970s, core questions on community
dynamics were addressed by ecologists using multivariate
approaches to describe temporal changes in real communities
(Allen and Skagen 1973; Allen et al. 1977) visualized in
ordination biplots as trajectories to track changes or identify
multiple stable points. Austin (1977) subjectively described
‘‘reversals of trends’’ on ordination biplots of plant communities. Subsequent studies on many different communities also
used trajectories in multivariate space to assess community
stability (Bloom 1980; Santos and Bloom 1980; Hughes 1990;
Vieira et al. 2004; Magalhães et al. 2007), identify alternative
community states (Warwick et al. 2002; Daufresne et al.
2007), or detect changes after perturbation (Boulton et al.
1992; Adjeroud et al. 2009; Muehlbauer et al. 2011).
These and other studies revealed a broad spectrum of
community changes in response to various underlying
mechanisms, with trajectory patterns including both smooth
or ‘‘gradual’’ and abrupt or ‘‘saltatory’’ changes, and patterns
of change that were either directional or non-directional
(idiosyncratic). We propose that scenarios of community
change can be visualized in a cross-classified framework
(Fig. 1) in which a community could change: (1) by gradual
steps or by saltatory changes; and (2) either (a) idiosyncratically, (b) directionally persistent, or (c) directionally but
followed by return toward a previous state. See Smith (2012),
Lake et al. (2007), or Mittlebach et al. (2006) for other
hypothetical patterns related to community change or
recovery from a stressor. First, in our scheme a community
may be characterized by idiosyncratic changes (Drake 1991;
Matthews and Marsh-Matthews 2006a), and lack an overall
directional trajectory in multivariate space (Fig. 1a, d). A
community characterized by gradual variation exhibits regular increments of change (Fig. 1a–c), with directional
change, if any (Fig. 1b, c), that could result from a chronic
‘‘press’’ disturbance (Lake 2000), or from long-term turnover of species (Magurran and Henderson 2010). In contrast,
a predominantly event-driven community (Fig. 1d–f) may
show little change until ‘‘pulse’’ or ‘‘ramp’’ events (Lake
2000) or an experimental treatment (Muehlbauer et al. 2011)
result in a relatively large, saltatory move (Sponseller et al.
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2010). Regardless of the drivers, community changes may be
directional (Collins 2000), diverging overall from the original state, or not. Saltatory changes may be directional
(Fig. 1e, f), to an alternate community state (Scheffer and
Carpenter 2003; Paine and Trimble 2004) differing markedly
from the original structure. And after either gradual or eventdriven change to a new state (Fig. 1b, c, e, f), a community
may subsequently return toward its previous condition
(Fig. 1c, f) as exemplified by Eby et al. (2003) and Muehlbauer et al. (2011), or remain in a stable alternative state
(Fig. 1b, e) as shown in Daufresne et al. (2007) and Rodriguez et al. (2003). A community may not exclusively fit
either a gradual or an event-driven model, as real communities can show both gradual and rapid changes at various
times (Warwick et al. 2002; Daufresne et al. 2007), and
return toward a previous state can be partial (Gardner and
Wear 2006) or complete (Muehlbauer et al. 2011).
It is unlikely that any real-world community will conform precisely to any one of the six patterns we propose in
Fig. 1, given sufficient time for disturbances of different
magnitudes or random events affecting recruitment of
species. But these patterns should provide a point from
which to view long-term changes in natural communities,
ask questions about underlying drivers, or help inform
focused experiments on potential biotic (e.g., life history)
or abiotic (environmental) drivers of change. As a first test
for the generality of the hypothetical patterns (Fig. 1), we
reviewed a total of 71 multivariate trajectories appearing in
27 published papers (ESM1) on a wide variety of taxa, not
including the trajectory of the system (Brier Creek, Oklahoma, USA) that is the focus of this paper. All of the
hypothetical trajectories in Fig. 1 were exhibited by at least
some of the communities we reviewed. In 23 of the 71
trajectories there was at least one saltatory directional
change, followed by recovery toward pre-change conditions (Fig. 1f). Another 19 exhibited at least one period of
directional saltatory change but no return toward an earlier
state (Fig. 1e). Thus, 42 of 71 (=59 %) of the trajectories
showed at least one saltatory change. Five other trajectories
had one or more saltatory changes, but no overall directional change in multivariate space (Fig. 1d). In the other
29 trajectories change was by gradual increments whether
directional (15 cases; Fig. 1b) or not (six cases; Fig. 1a), or
whether there was any pattern of return toward an earlier
state (three cases; Fig. 1c). Thirty-four trajectories were
directional without return, whereas 26 were directional in
part but with subsequent return toward an earlier state.
Thus, this review of temporal trajectories suggests a wide
variety of community responses to manipulation, natural
disturbance, or mere passing of time, but more than half
showed saltatory change(s), and the majority showed a
tendency to return to a former state if displaced, supporting
the earlier concepts of Lewontin (1969) and May (1973) of
Oecologia
b
c
d
e
f
Saltatory
Gradual
a
Non-directional
Directional
Directional with
return
Fig. 1 Hypothetical trajectories of temporal change in communities,
depicting temporal movement of a community through multivariate
species-space, as might be analyzed using non-metric multidimensional scaling (NMDS), correspondence analysis, or detrended
correspondence analysis plots. The framework depicts gradual versus
saltatory change crossed with non-directional (idiosyncratic), directional, or directional change with return. Saltatory changes could
result from stochastic events like floods or droughts, whereas return
toward a previous community state might result from deterministic
processes. Trajectories include a gradual, non-directional; b gradual,
directional; c gradual, directional with return; d saltatory, nondirectional; e saltatory, directional; f saltatory, directional with return.
The black dot represents the first of 15 sequential surveys of a
hypothetical community
communities lying within some probabilistic ‘‘cloud of
points,’’ and Collins’ (2000) concept of communities in
general showing ‘‘loose equilibrium.’’ It is in this light that
we assess the Brier Creek fish community, over four decades, to test applicability of our framework in a system
in which some of the most extraordinary, and repeated,
disturbances (flood and drought) on record have occurred.
To test predictions of any theoretical constructs about
communities, long-term empirical studies are extremely
valuable (Magurran et al. 2010). Long-term studies can
detect patterns that only develop across generations of
organisms. Connell and Sousa (1983) emphasized that
studies of community dynamics should be long enough to
allow at least one complete turnover of all individuals in
the original community. Long-term studies are also more
likely to include natural disturbances of differing kinds or
intensities (Bêche and Resh 2007) such as unpredictable,
rare, catastrophic disturbances like extreme floods (Matthews 1986; Thibault and Brown 2008), extraordinary
droughts (Lake 2011), or hurricanes (Lugo et al. 2000;
Willig et al. 2011; Geheber and Piller 2012) that can be
major agents of community change or have non-linear
effects (Brown and Ernest 2002; Turner et al. 2003). Longterm studies can help identify the relative importance of
different community-organizing processes (Grossman and
Sabo 2010).
Numerous recent studies at the scale of multiple decades
(20 years or longer) are on communities including phytoplankton, zooplankton, corals, stream invertebrates, intertidal or benthic marine communities, fishes, salamanders,
small mammals and birds (Elliott 1990; Hairston and
Wiley 1993; Cody and Smallwood 1996; Coppedge et al.
2001; Warwick et al. 2002; Eby et al. 2003; Paine and
Trimble 2004; Wakeford et al. 2008; Gido et al. 2010;
Magurran and Henderson 2010; Thibault et al. 2010).
However, questions that still beg for generalization across
long-term studies of communities include:
1.
2.
3.
4.
What is the relative importance of ‘‘event-driven’’
versus gradual change (Mittlebach et al. 2006; Jentsch
et al. 2007)?
Do communities typically change states (Scheffer and
Carpenter 2003) after some threshold is reached
(Dodds et al. 2010) or after catastrophic disturbance
(Carpenter et al. 2011)?
Do communities follow long-term directional trajectories (Collins 2000; Muehlbauer et al. 2011) that can
be related to species-specific life history or physiological traits?
What are the effects of repeated disturbances over
short periods of time?
Here, we address the dynamics of the Brier Creek fish
community over a span of 40 years, and test hypotheses
about observed changes as related to disturbance. This is
one of the longest available datasets for a stream fish
community. During our study period, Brier Creek had three
extraordinary disturbance events, including the worst erosive flood on record for the watershed and extreme
droughts only 2 years apart, along with numerous other
erosive floods and dry periods. We document variation in
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the fish community in 16 surveys from 1969 to 2008 and
use 14 surveys we personally conducted from 1981 to 2008
to test hypotheses about drivers in the dynamics of the fish
community. Thus this multi-decade data set provides the
opportunity to: (1) assess long-term qualitative and quantitative variation in a real community; (2) test the
hypothesis of more change than at random in response to
disturbance events in general, or to events of extreme
magnitude; and (3) test whether, after event-driven change,
the community returned toward an earlier, ‘‘typical’’ condition (as opposed to remaining in an alternate state). We
also evaluated mechanisms of the observed changes as
related to life history or behavioral traits of individual
species, or to changes in abundance of particular trophic
groups (particularly for predators and potential prey), and
compared the observed trajectory of the Brier Creek fish
community to the hypothetical patterns in Fig. 1.
Materials and methods
Study area
Brier Creek (33°N, 98°W) is a small, clear, gravel-bed
stream, mostly with riffle-pool structure, draining
59.6 km2, with a main stem approximately 20 km long, in
Marshall County, south-central Oklahoma, USA (Fig. S1,
ESM2). The shallow headwaters are mostly in open pasture
lands dominated by cattle grazing, whereas the lower main
stem is characterized by deeper pools, incised in earthen
banks several meters high and surrounded by riparian forest
(ESM2). Flow is often interrupted in the headwaters during
dry spells, but the lower main stem flows perennially
except in the worst droughts. Brier Creek is a direct tributary of Lake Texoma, a large manmade reservoir
impounded on the Red and Washita rivers in 1947. The
watershed is entirely rural, with little change in land use
since the initial fish survey in 1969 (Smith and Powell
1971; Matthews and Marsh-Matthews 2007). The region
has hot summers and cold winters, with 97 cm average
annual precipitation, and the Brier Creek watershed is
characterized by a generally harsh, fluctuating environment
(Ross et al. 1985; Matthews 1987).
Brier Creek is prone to erosive floods, with rapid stage
rises of 4.5 m or more, and peak calculated discharges as
much as 55 m3/s (Harvey 1987; Power and Stewart 1987;
Matthews et al. 1994; Wesner 2011), and velocity
approaching 2 m/s (W. J. M., field notes). These floods
move the stream bed, scour or deposit gravel to form or fill
pools, and undercut stream banks, causing logs or whole
trees to be swept downstream (Harvey 1987; Power and
Stewart 1987). The creek also has a history of extreme
droughts, with fish crowded into tiny isolated pools or
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eliminated from headwater sites (Matthews 1987; Matthews and Marsh-Matthews 2003, 2007, 2010). Eight of the
13 intervals between our 1981–2008 surveys and the
interval before the 1981 survey included severe to extreme
events, including erosive floods, droughts, or both (ESM2).
We subjectively classified four of the events as ‘‘extreme’’
relative to all others based on climate records and our own
field observations (ESM2).
Extreme events included: (1) drought in summer 1980
(Palmer Z short-term drought index = -3.90, http://
climate.ok.gov) with extremely high temperatures, resulting in direct heat death of some fishes (Matthews et al.
1982; Ross et al. 1985); (2) a massive flood in October
1981 due to 66 cm of rain in 7 days, with 26 cm in 3 day;
(3) the worst drought on record in summer 1998 for SouthCentral Oklahoma Climate Division (Palmer Z = -4.42);
and (4) a locally extreme drought in summer 2000, with no
measurable rain in Marshall County in August (MarshMatthews and Matthews 2010).
Brier Creek is a good model for other small streams.
Evidence from collections included in this paper and other
ancillary sampling (W. J. M., E. M. M., unpublished data)
indicates that the system is open to immigration of fishes
from the reservoir (ESM3), and that temporal changes in
the fish community are similar in magnitude to changes in
other streams in southern Oklahoma (ESM3). Thus, Brier
Creek is a system that may relate well to other small
streams in rural or agricultural regions of the southern
United States. And, due to extensive reservoir building in
the latter half of the 20th century in the United States
(Baxter 1977) and worldwide (Nilsson and Berggren 2000),
many small streams are now direct tributaries to man-made
reservoirs (e.g., Falke and Gido 2006), so findings from
Brier Creek may be pertinent to many other streams that
flow directly into large reservoirs.
Fish sampling: history and technique
History of all surveys, details of sampling, and validation
of sampling methods are in ESM4. Brier Creek has a long
history of fish community surveys (Smith and Powell 1971;
Ross et al. 1985; Matthews et al. 1988; Matthews and
Marsh-Matthews 2006b) and ecological studies of fishes
(Power and Matthews 1983; Gelwick and Matthews 1992),
which provide detailed descriptions of the watershed or
floods and droughts. Brier Creek is characterized by native
fishes that are tolerant of physicochemical stressors (Matthews 1987). The earliest known, but unpublished, fish
collection in Brier Creek was at one downstream site by
Carl Riggs in July 1950 (C. Riggs, field note R50-9, Sam
Noble Oklahoma Museum of Natural History). The first
comprehensive fish survey of the watershed was by Smith
and Powell (1971), in summer 1969 at six fixed sites. In
Oecologia
1976 Echelle and class (W. J. M. participated) surveyed
fish at five of Smith and Powell’s sites, and at one new
headwater site (Fig. S1, ESM1). We (the present authors)
sampled those six sites in 14 summers from 1981 to 2008,
with the exception that in 1988 the uppermost site was dry,
so only five sites were sampled. The 1981–2008 surveys
were directed by W. J. M. with the exception of 1986 and
1995, and there was cross-participation of all authors in
various surveys (Table 1). Sampled stream reaches were
200- to 500-m (mean = 360 m) long (site descriptions in
ESM2). Our goal was to sample all species in proportion to
their abundance, in all available microhabitats such as open
pools, undercut banks, root wads. woody debris, and vegetation. We used seines 4.6 m long 9 1.2 m deep with 4.5mm mesh in pools, with shorter seines of similar mesh (to
1.8 m long) for kick sets in flowing riffles or in narrow
headwaters channels where shorter seines were more efficient. Fish were preserved for enumeration in the laboratory with the exception that large-bodied adults were often
identified, recorded and released. Our 1981–2008 samples
are archived in the Department of Ichthyology, Sam Noble
Oklahoma Museum of Natural History. We followed
Matthews (1998, as modified from numerous sources) to
classify Brier Creek species into trophic groups based on
their primary diet as adults (Table 1), to compare temporal
changes among groups.
Data analyses
Data were pooled across the six fixed sites to form a
composite community data set for Brier Creek in each
survey year (Table 1). Habitats in Brier Creek range from
the small, harsh headwaters sites to the larger, lower main
stem (Matthews 1987), resulting in distinct longitudinal
differences in fish species distributions (Smith and Powell
1971; Ross et al. 1985; Matthews 1987). However, the
focus here is on the ‘‘big picture’’ of long-term dynamics of
the total fish community of the watershed, and detailed
analysis of longitudinal patterns or site-specific temporal
changes will be the subject of future papers, as additional
long-term data are gathered. For the composite survey data,
we followed Ross et al. (1985) and calculated mean total
abundance (Table 1) of each species across seven sampling
dates in 1969 by Smith and Powell (1971), and across two
samples in June and July 1981 by W. J. M. From 1969 to
2008 a total of 32 species was detected (Table 1). We used
Jaccard’s index (JI) to estimate species turnover among
surveys. For multivariate analyses we omitted species that
occurred only once, or totaled five or fewer individuals
across all surveys (Table 1). We limited the multivariate
analyses on the 23 remaining species to the surveys we
directed from 1981 to 2008, for which we have personal
information on antecedent environmental events.
For multivariate analyses, we converted abundances to
log10(x ? 1), improving linearity among some species
pairs and lessening the potential influence of highly
abundant species. With log-transformed data, we initially
compared five resemblance metrics and three ordination
methods that are commonly used in community ecology
(ESM5). The multivariate analysis in the ‘‘Results’’ is
based on the Bray-Curtis distance (BCD) among surveys
followed by non-metric multidimensional scaling (NMDS).
We also used BCD to quantify changes in the fish community between individual surveys. BCD was not autocorrelated between consecutive surveys [Wessa 2012; free
statistics software version 1.1.23-r7; autocorrelation at lag
1, with white noise time series: ACF (k) = 0.259,
P = 0.18]. To provide comparative ordination methods,
we also carried out correspondence analysis (CA), and
detrended correspondence analysis (DCA), which are
commonly used in community ecology, on the 1981–2008
data. Results of CA and DCA were similar to NMDS with
respect to trajectories, temporal trends, and effects of
drought, so biplots of CA and DCA are shown only in
ESM6.
Calculations of BCD and all ordinations were by PCORD version 6. For NMDS of the triangular BCD matrix
we first used the step down option of PC-ORD from six
to two axes, without the autopilot option, and used a
scree plot to determine optimal stress versus number of
axes. The best solution was a two-dimensional solution,
and we used the weighted averages option in PC-ORD to
position species centroids on the two NMDS axes. We
used the first final two-dimensional run of the NMDS for
results, but we also re-ran the two-dimensional NMDS
several additional times as recommended by McCune and
Grace (2002). Results were similar each time, so the
NMDS should be a stable solution, not affected by local
minima (McCune and Grace 2002). Following the
approach of Hughes (1990) we used a clustering classification analysis to objectively delineate post hoc groups
of surveys on the NMDS biplot. For this we did a
unweighted pair group method with arithmetic mean
(UPGMA) cluster analyses based on BCD between all
pairs of surveys, in PC-ORD.
To determine if some surveys were more extreme on the
NMDS biplot than was likely at random, or if BCD
between some consecutive surveys were larger than random, we used the Monte Carlo algorithm of Schaefer et al.
(2005) (program obtained from Ecological Archives A015052-S1), as detailed in ESM7.
To test for evidence that events caused saltatory change,
we compared BCD to numbers of events (drought, flood, or
both; ESM2) by Spearman rank correlation. We also used
Mann–Whitney tests to compare BCD between: (1) intervals that included ‘‘events’’ (of either kind) versus those
123
Trophic
group
BO
A
H
IO
IO
IO
IO
IO
IO
IO
BO
BO
BI
BI
O
O
P
IO
IO
IO
IO
P
P
P
P
IO
IO
IO
M
P
P
BI
BI
Scientific name
Cyprinus carpioc
Campostoma anomalum
123
Ctenopharyngodon idellac
Cyprinella lutrensis
Cyprinella venusta
Notemigonus crysoleucas
Notropis boops
Notropis stramineus
Pimephales promelas
Pimephales vigilax
Carpiodes carpioc
Ictiobus bubalusc
Minytrema melanops
Moxostoma erythrurum
Ameiurus melas
Ameiurus natalis
Ictalurus punctatusc
Gambusia affinis
Labidesthes sicculusc
Menidia beryllinac
Fundulus notatus
Micropterus punctulatus
Micropterus salmoides
Lepomis cyanellus
Lepomis gulosusc
Lepomis humilis
Lepomis macrochirus
Lepomis megalotis
Lepomis microlophus
Pomoxis annularisc
Pomoxis nigromaculatusc
Etheostoma spectabile
Percina macrolepida
2
63
0
1
0
26
4
0
1
6
5
4
10
0
3
0
0
5
0
0
0
0
0
2
6
14
0
0
2
34
0
14
0
Riggs
1950a Site6
1
61
0
0
1
141
16
28
0
45
6
19
64
1
2
1
0
8
4
0
0
0
1
19
57
0
669
2
3
124
0
68
1
Smith and
Powell 1969b
Table 1 Species collected in Brier Creek, Marshall County, Oklahoma, USA
0
86
0
0
0
44
9
22
0
54
2
1
25
0
0
102
0
1
8
2
0
0
0
3
0
0
233
1
35
9
0
205
0
Echelle
1976 WJM
3
166
0
1
23
56
67
65
0
125
45
0
24
0
0
19
1
2
0
0
1
0
1
10
19
0
82
26
73
158
0
165
0
1981
WJM
65
160
1
0
6
216
106
41
0
665
102
1
19
0
0
4
0
22
7
0
3
0
1
7
5
4
424
13
42
129
0
600
0
1985
WJM, FG
4
12
0
0
7
60
61
7
0
155
47
0
41
0
0
0
0
0
15
0
0
0
0
2
0
0
901
4
43
232
0
218
0
1986
RCC
9
1,193
0
0
15
190
61
28
0
126
471
10
137
0
0
0
0
9
8
10
2
0
1
12
0
6
184
1
34
119
0
2194
0
1988
WJM
2
327
0
1
23
303
94
17
0
535
16
20
122
0
0
14
0
3
5
4
0
0
1
22
0
1
1,114
1
13
22
0
228
0
1991
WJM, FG
0
122
0
0
34
197
191
15
0
167
40
10
53
0
0
0
0
4
26
1
0
0
0
24
0
8
405
2
72
41
0
556
0
1993 WJM,
RCC, FG
Oecologia
0
0
0
0
0
0
0
1
0
0
0
1,628
3,408
0
61
0
0
7
414
156
0
0
217
42
21
703
0
0
248
0
5
4
2
0
0
0
11
0
1
1,399
0
8
33
0
75
0
1996 WJM, RCC, FG
1,822
2
472
0
0
5
311
64
1
0
34
405
8
63
0
0
13
0
6
1
3
3
0
0
0
0
0
317
1
0
0
3
110
0
1999 WJM
4,400
2
588
0
1
11
76
54
136
0
457
460
84
15
0
0
13
0
35
2
291
238
0
0
2
0
4
508
11
0
8
0
1,397
1
2001 WJM, EMM
3,136
2
544
0
0
12
179
72
19
0
427
64
122
32
0
0
0
0
15
20
89
37
0
0
2
30
13
162
7
0
1
0
1,272
0
2002 WJM, EMM.
3,856
16
399
0
0
30
451
143
3
0
559
161
27
242
0
0
15
0
5
19
28
1
0
0
0
1
119
911
23
16
7
0
678
0
2004 WJM, EMM
3,403
0
67
0
0
23
166
95
10
0
523
117
56
97
0
0
0
0
4
0
20
4
2
0
0
7
10
383
23
28
71
0
1,693
0
2008 WJM, EMM
c
b
a
Omitted from multivariate analyses
Smith and Powell (1971)
C. Riggs, field note R50-9, Sam Noble Oklahoma Museum of Natural History
BO Benthic omnivore, A Algivore, H herbivore (on macrophytes), IO insectivore/omnivore, BI benthic insectivore, O omnivore, P piscivore, M molluscivore
Initials following collection year indicate which of the authors participated in that collection
2,279
5
137
0
0
225
3
62
106
195
169
120
43
41
12
51
118
10
13
0
9
0
0
0
0
34
0
0
0
0
1
1
2
7
24
0
0
0
2
13
11
856
0
0
35
72
63
523
0
94
22
139
0
1995 RCC, FG
0
667
0
1994 WJM, RCC, FG
Table 1 continued
11
16
1
3
15
16
16
14
16
16
14
16
1
1
11
2
14
14
11
8
1
5
13
6
11
16
13
13
15
1
16
2
Occurrences 1969–2008
Oecologia
123
Oecologia
Results
Overall variation in the community
In 1950, Riggs recorded 18 species at one Brier Creek site
(Table 1), of which we collected 16 from 1981 to 2008.
The two species in Rigg’s sample we did not find from
1981 to 2008 were brook silversides (Labidesthes sicculus),
which Riggs in 1950 and Smith and Powell (1971) in 1969
detected in very low numbers, and warmouth (Lepomis
gulosus), which we did not collect from 1981 to 2008.
However, in additional sampling at two sites after 2008 we
(W. J. M., E. M. M., unpublished data) subsequently
found several warmouth. As another indicator of the low
turnover of species across time in Brier Creek, 28 species
were detected in sampling six sites throughout the watershed by Riggs, Smith and Powell, or Echelle from 1950 to
1976, or in our surveys in the 2000s (Table 1), with 24
shared between the early surveys and ours of the 2000s
(JI = 0.887). In our 1981 survey we detected 22 species,
and found 20 of them again in the 2000s (JI = 0.952). The
two species from 1981 we did not find in the 2000s were
river carpsucker (Carpiodes carpio) and channel catfish
(Ictalurus punctatus) for which we found only one each in
1981.
Eight species that occurred in all 16 of the system-wide
surveys from 1969 to 2008, and nine other species that
were detected in most (13–15) surveys (Table 1) comprised
a core of 17 species in Brier Creek. Six other species were
123
detected in six to 11 surveys, for a total of 23 species
common in the Brier Creek community. Nine species were
detected only rarely (Table 1), including large-bodied
species and two silversides that were likely strays from
Lake Texoma, and one exotic (grass carp, Ctenopharyngodon idella, that is frequently stocked in ponds for weed
control). One species (sand shiner, Notropis stramineus)
not found in our surveys until 1985, became established
and occurred in ten of 12 subsequent surveys (Table 1). No
abundant species in Brier Creek disappeared completely
during the study, although several showed sharp declines
(Table 1). The most common species varied markedly in
abundance in various surveys, but not synchronously
(Table 1).
The most abundant trophic groups were water column
insectivore-omnivores (minnows, topminnows, smallmouthed Lepomis sunfishes, and western mosquitofish,
Gambusia affinis), and piscivores (including largemouth
bass, Micropterus salmoides, and spotted bass, Micropterus
punctulatus, and large-mouthed Lepomis sunfishes)
(Table 1). From 1969 to 2008 the percentage of species
that are piscivores as adults increased (Pearson r of piscivores vs. years = 0.505, P = 0.046), and water column
insectivores and insectivore-omnivores decreased (r =
-0.462, P = 0.072), resulting in a strong negative relationship (Pearson r = -0.630, P = 0.009) between these
trophic groups (Fig. 2).
Community trajectory in multivariate space
We focus on the position of individual surveys and the
temporal trajectory of the community in the NMDS biplot
(Fig. 3a) to summarize long-term trends in Brier Creek.
Our 1981 survey, which was located at the far left on axis 1
100
Insectivore-Omnivores (%)
that did not, (2) intervals that did or did not include flood,
and (3) intervals that did or did not include drought.
If community change is directional over time, biplots
should exhibit a trend for progressive divergence of surveys from the initial state. On the NMDS biplot we counted
the number of movements away from versus back in the
direction of the community in our first (1981) survey. We
also followed Hughes (1990) and used the angles of
movements between consecutive surveys in the NMDS
biplot to ask if, in each step, the community continued to
move further away from the previous position, or back
toward it. If the angle of the trajectory from time 1 to 2 to 3
is obtuse ([90°) then the community is continuing to move
further away from the point represented by time 1, whereas
acute angles (\90°) represent movement back toward time
1, not contributing to an overall directional trajectory. We
also compared each survey to our initial survey in 1981,
and tested for increases in BCD with years since the initial
survey by linear regression, followed by a runs test (PASW
Statistics 18, 2007) of increasing versus decreasing BCD
values relative to 1981 to identify trends during any particular time periods.
80
60
40
20
0
0
5
10
15
20
25
30
35
Piscivores (%)
Fig. 2 Percentage of insectivore–omnivores versus percentage of
piscivores in Brier Creek in each survey of 1969–2008
Oecologia
a
1.5
2002
1.0
2001
2008
0.5
1981
1985
1988
2004
0.0
-0.5
1999
1994
1993
1991
1986
-1.0
1996
1995
NMDS 2
of the NMDS (Fig. 3a), followed an unusually hot, dry
summer in 1980 (Ross et al. 1985; Online Resource 1). The
1985 survey moved toward the middle of the biplot, but not
with an unusually large BCD, even though the most
extreme flood (October 1981) and other dry periods and
floods were in that interval (ESM2). From 1981 up to and
including 1994, surveys were in relatively limited space to
the left in the biplot (Fig. 3a). Then in 1995 and 1996 the
trajectory moved downward on axis 2. (Note that axes in
NMDS biplots are of equal importance, thus movement in
any direction on the biplot can be considered equally
important, biologically.) Between the 1996 and 1999 surveys, the worst drought to that date for Marshall County
occurred (in 1998; Matthews and Marsh-Matthews 2006b),
and the 1999 survey was markedly displaced to the right
side of the NMDS biplot. A second exceptional drought
occurred in summer-fall 2000 (Matthews and Marsh-Matthews 2006b, 2010), and the survey in 2001 showed
another large displacement in NMDS space, upward on
axis 2. The movements of surveys in NMDS space in 1999
and in 2001, after two extreme droughts in close succession
(1998 and 2000), were the largest for any intervals between
surveys (Fig. 3a), and these intervals had the two largest
BCD values (0.245 and 0.242, respectively) for any intervals between surveys. Then, from 2002 through 2008 the
community moved back toward a long-term average condition. UPGMA clustering (ESM6) of the surveys based on
BCD values reinforced these interpretations by showing
two distinct clusters at a BCD of 0.27 that included: (1)
1999, 2001, and 2002; and (2) all other surveys, including
those in 2004 and 2008. But if a cutoff for clusters is placed
at approximately BCD = 0.21 in the UPGMA tree
(ESM6), five subclusters can be identified, with 1981 to
1986 as one subcluster; 1995 and 2001 each as a sole
member of a separate subcluster; 2001 and 2002 as a
subcluster; and, importantly, the surveys of 2004 and 2008
occurring in a subcluster with most of the other years in the
middle of the NMDS plot. In other words, the UPGMA
clustering (ESM6), whether we use a BCD cutoff of 0.21
(giving five subclusters) or 0.27 (giving two major clusters), shows the years 2004 and 2008, subsequent to the two
extreme droughts of 1998 and 2000, to have moved back
toward a typical Brier Creek community structure, i.e.,
closer to the middle of NMDS space (Fig. 3a).
Monte Carlo simulations showed that three of the annual
surveys were more different from the long-term average
community than was likely at random (1986, P = 0.004;
1995, P = 0.003; 1999, P = 0.003), and a fourth survey
(1996) was marginally different at P = 0.09. Monte Carlo
simulations starting with real abundances for 1996 and,
separately for 1999, showed that the BCD from 1996 to
1999 was significantly larger than at random (P = 0.04),
and the BCD from 1999 to 2001 differed from random at
-1.5
-1.5
-1.0
-0.5
0.0
0.5
1.0
1.5
1.5
2.0
b
1.0
MM
PP
NC
LH
PM
0.5
0.0
CL
CV
ME
AN
MP
GA
PV
-0.5
-1.0
-1.5
-1.5
-1.0
-0.5
0.0
0.5
1.0
1.5
2.0
NMDS 1
Fig. 3 NMDS, based on Bray-Curtis distances, for Brier Creek
surveys from 1981 to 2008, based on 23 species, with a survey scores
indicated on axes 1 and 2, and b species overlaid on the same NMDS
axes. Of the 23 species, 11 formed a highly overlapping cluster in the
center of the NMDS plot, which are not individually identified in b.
Species outside this core are indicated as follows: Cyprinella lutrensis
(CL), Cyprinella venusta (CV), Notemigonus crysoleucas (NC),
Pimephales promelas (PP), Pimephales vigilax (PV), Minytrema
melanops (MM), Moxostoma erythrurum (ME), Ameiurus natalis
(AN), Gambusia affinis (GA), Micropterus punctulatus (MP), Lepomis
humilis (LH), Percina macrolepida(PM). Species in the core are
identified in Fig. S10 (ESM)
P = 0.09. The difference between surveys in 1996 and
2001 (which spanned the two severe droughts), was greater
than the difference for any single interval, with
BCD = 0.317, and a Monte Carlo simulation beginning
with the 1996 data showed that the difference between
1996 and 2001 was much greater (P \ 0.001) than would
have occurred by random fluctuations in species
abundances.
The Brier Creek NMDS biplot (Fig. 3a), judged by the
same criteria we used for the 71 trajectories we classified
by our hypothetical framework (Fig. 1; Online Resource
1), showed two (or possibly three) intervals with saltatory
change (1986–1988, 1996–1999, and 1999–2001), and
each of these intervals also had a large BCD. Each of these
123
Oecologia
intervals included a severe drought (1996–1999,
1999–2001) or was a survey made during a severe dry
period (1988). We also saw evidence of the trajectory after
2001 returning back toward an earlier state, e.g., toward the
center of the biplot and/or toward the first survey in 1981,
so we judged the overall pattern to show ‘‘return.’’ Thus,
we classified Brier Creek as having ‘‘saltatory change,
followed by return,’’ most nearly fitting hypothetical pattern F in Fig. 1.
a
Influence of individual species on multivariate analyses
Testing for event-driven change and directional
community trajectory
If change is gradual, not event driven, differences among
surveys could be a simple effect of ‘‘time.’’ But there was
no correlation between BCD and numbers of years between
surveys (Spearman’s q = 0.083, P = 0.786), and no significant correlation between BCD and number of events in
an interval (Spearman’s q = 0.101, P = 0.744). Viewed
by occurrence of different type(s) of events (regardless of
number in an interval), there was a trend for more change
123
b
Bray-Curtis distance
Notable trends that relate to positions of the surveys in the
NMDS biplot (Fig. 3a) included: maxima for western
mosquitofish in 1976 and 1996; major increases in largemouth bass, golden redhorse (Moxostoma erythrurum),
spotted sucker (Minytrema melanops), and orangethroat
darter (Etheostoma spectabile), following extreme droughts
in 1998 or 2000; and declines in red shiner (Cyprinella
lutrensis), and blacktail shiner (Cyprinella venusta) in
recent surveys (Table 1). The overlay of species weighted
averages on the NMDS axes (Fig. 3b; Fig. S10 in ESM6)
suggested that movement of the 1995 survey toward the
lower left in the biplot coincided with a decrease in numbers
of central stonerollers (Campostoma anomalum), low
numbers of black striped topminnows (Fundulus notatus),
and relatively high numbers of red shiners and blacktail
shiners. Movement of the 1996 survey toward the right on
axis 1 coincided with the largest numbers of mosquitofish
and topminnows in any of our surveys (Table 1). In 1999,
following the extreme drought of 1998, the large move of
the community to the right and upward on the NMDS biplot
coincided with a large increase in largemouth bass and loss
of red shiners and blacktail shiners (Table 1). Then, after the
severe drought in 2000, the surveys in 2001 and 2002 were
in the upper part of NMDS axis 2 (Fig. 3a), reflecting
increases in the two suckers: golden redhorse and spotted
sucker (Table 1). But by 2004 and 2008 abundances of the
suckers and bass decreased, red and blacktail shiners were
again found (Table 1), and the community moved back
toward the middle of the biplot.
c
Fig. 4 Boxplots comparing Bray-Curtis distances between consecutive surveys in intervals without (NO) and with (YES) a flood and
drought events, b floods, and c droughts
(larger BCD) in intervals with either flood or drought relative to intervals with no events (Fig. 4a); no effect of
floods alone (Fig. 4b); but a significant effect of drought
alone (Fig. 4c) relative to all intervals lacking drought
(Mann–Whitney U = 7.00, P = 0.05, MedCalc version
11.2.1). In addition, the largest BCD values corresponded
to two intervals (1996–1999, 1999–2001) with the most
extreme droughts during our study period.
A runs test (PASW statistics) of the increase or decrease
of Bray–Curtis distances between the 1981 survey and all
surveys 1985–2008 (Fig. 5) was non-significant
(P = 0.999), reinforcing the finding that there was no
Oecologia
0.32
Bray-Curtis distance
relative to 1981
0.30
0.28
0.26
0.24
0.22
0.20
0.18
0.16
0
5
10
15
20
25
30
Years since 1981
Fig. 5 Bray-Curtis distances comparing each survey to the survey in
1981, versus number of years since 1981
overall directional trend away from the initial community
state. BCD versus years since 1981 (Fig. 5) suggested a
general trend away from the initial survey until the period
1999–2002, followed by a distinct reversal in 2004 and
2008, with the BCD for those intervals relative to 1981
becoming smaller, indicating a return toward an average
community state. In the Brier Creek NMDS trajectory
(Fig. 3a) there were eight acute angles, compared to four
obtuse angles, indicating a lack of overall directionality. In
the biplot six surveys (not including 1985, which could
only move away from the starting point of 1981) moved
further away from the 1981 survey, and six moved closer to
1981, also indicating no overall directional displacement of
the community.
Discussion
Long-term variation in Brier Creek
Qualitative changes in the Brier Creek community were
relatively small over almost 60 years, since the first known
collection in 1950. Core species (e.g., Magurran and
Henderson 2010) were nearly always present from 1969 to
2008. Qualitative variation among surveys was mostly due
to rare, non-persistent transients presumed from Lake
Texoma. Only one new species became established from
1981 to 2008, and no species that was common in the
earlier surveys disappeared completely. Most species that
were detected in early samples remained present in the
watershed in recent surveys, indicating substantial qualitative stability in fish community composition, or high
‘‘persistence’’ sensu Connell and Sousa (1983).
Quantitatively, individual fish species in Brier Creek
showed substantial variation in abundance but interspecific
population fluctuations were asynchronous and most
species tended to return toward average values after years
of peak abundance, varying around their mean, as did
fishes in Magurran and Henderson (2010). There were
noteworthy changes in abundance between some trophic
groups, e.g., an increase in piscivores coincided with a
decline in water column insectivorous minnows. But
changes in these trophic groups did not result in long-term
change in community composition from the earlier state to
one persistently different.
We conclude that the Brier Creek fish community trajectory is closest to our hypothetical pattern in Fig. 1f, i.e.,
that the community did show saltatory change after two
extreme droughts, but transiently, with return toward an
average community state. This return toward a more
average state suggested long-term stability as defined by
Bêche and Resh (2007) or a loose equilibrium (Collins
2000). It seems noteworthy that the two extreme droughts,
with only one wetter year in between, caused large, nonrandom displacement of the Brier Creek fish community in
multivariate space. And effects of individual droughts may
be idiosyncratic: our surveys in 1985, 1988, and 2008, each
following or during a drought period, showed no consistent
amount or direction of movement of the community in
NMDS space. We suspect that the two temporally close,
extreme droughts of 1998 and 2000 were unique in their
degree of impact on the Brier Creek community.
In response to extreme events, other stream fish communities have shown many different responses, including
resistance to change (Meffe and Minckley 1987), rapid
recovery to a pre-event state (Matthews 1986; Franssen
et al. 2006), or change to a persistent altered structure
(Strange et al. 1993). Effects may differ among taxonomic
or ecological groups (Matthews et al. 1994; Marsh-Matthews and Matthews 2010) or among individual species
(Wesner 2011). Long-term data by Magurran and Henderson (2010) for a complex estuarine fish community
suggest a similar pattern of considerable variation in species abundances or community properties from year to
year, yet stability in the overall community or in its core
species (i.e., no directional change in structure) over a span
of 30 years. Other long-term studies of fishes have shown
that several decades of change may be directional, but at
times communities may sharply reverse their trajectories,
and return toward an earlier state (Eby et al. 2003; Pyron
et al. 2006). Multivariate trajectories of community change
for other taxa ranging from macroinvertebrates to woody
plants have shown marked displacement following experimental treatments or disturbances, followed by return
toward pre-disturbance composition (Gardner and Wear
2006; Muehlbauer et al. 2011), and our assessment of 71
trajectories across numerous studies (ESM1) indicated that
such patterns are common. But there is not yet enough
evidence to allow a general consensus that changes in
123
Oecologia
stream fish communities (or communities in general) are
typically gradual, event driven, or idiosyncratic, thus, as
Jackson et al. (2001) indicated, the need remains for longterm data on more communities of all kinds.
There have, however, been a substantial number of
studies of freshwater fish communities spanning decades
(Eby et al. 2003; Beugly and Pyron 2010; Gido et al. 2010;
Stefferud et al. 2011; Penczak 2011) that underscore the
value of including sufficient time for the expression of
effects of events, whether natural or anthropogenic. And
events during the last decade of our own surveys support
the importance of long-term studies of communities. If our
surveys had ended in 1996, before the two extreme
droughts in 1998 and 2000, we might have concluded that
the Brier Creek fish community was characterized by
gradual, directional change away from its state in 1981, and
only minimally affected by disturbance events. Bêche and
Resh (2007) provided a similar cautionary note about
potentially false conclusions from short-term data. Our
continued surveys in the last decade allowed us to document responses to the two extreme droughts, and reach a
very different conclusion: that the community changed
rather gradually and somewhat directionally for approximately 15 years, until punctuated by event-driven changes
in trajectory, but after which the community reversed back
toward a more typical pre-disturbance condition. Without
the long-term data we would have completely overlooked
this important difference in dynamics of the system.
Mechanisms driving change and recovery
Hydrology is critical in stream systems (Sabo et al. 2010),
but fishes in Brier Creek (Matthews et al. 1994; Wesner
2011) or other streams (Meffe and Minckley 1987; Matthews 1986, 1998) may be less affected by flood than
drought, as adults in erosive floods typically find refuge
from strong currents. The great flood of October 1981 was
one of three ‘‘extreme’’ events in our study, but there was
little signal of its negative effects as of the next survey in
1985. And flooding can clean substrates of silts and expose
bedrock or gravel substrates, potentially favoring fish that
are egg attachers or gravel nesters. Floods in Brier Creek
can decimate fish larvae (Harvey 1987), but there is no
evidence that adults are washed out of the system. During
erosive flooding in Brier Creek adult fish typical of pool or
riffle habitats use low-velocity microhabitats along stream
edges or in flooded woods (W. J. M. field notes). Franssen
et al. (2006) and Wesner (2011) suggested that erosive
floods may actually facilitate recolonization of fish.
In our study, drought caused more changes in the fish
community than floods. Drought or dry periods can have
severe effects in both terrestrial (Frank and McNaughton
1992; Yahner 1992; Zeng and Qian 2005) and aquatic
123
ecosystems (Sabo and Post 2008; Sabo et al. 2010; Lake
2011). Droughts cause direct mortality of fish from
crowding in isolated pools, where water quality declines
and small fish become prey for larger species (Matthews
and Marsh-Matthews 2007), or result in many indirect or
residual effects (Matthews and Marsh-Matthews 2003). But
after drought, fish that survive may rapidly recolonize rewatered reaches (Franssen et al. 2006), and reproduce
successfully (Matthews 1987). Most common species in
Brier Creek are tolerant of high temperatures or low oxygen, common in isolated pools during drought (Matthews
1998). Our overall evidence, like that of trajectories in
Magalhães et al. (2007), suggest that after even severe
drought, fish communities will tend to recover over a
period of years back toward their earlier configurations.
However, our evidence suggests that consecutive severe
droughts (e.g., a second drought before the community has
recovered from the first) may intensify the effect on a fish
community beyond that of any single drought.
Differences among species in ability to resist stressors
like high temperature and low oxygen (Matthews 1987)
can result in differential survival in drought (Marsh-Matthews and Matthews 2010). After drought, survivors may
rapidly recover to body condition equal to (or greater than)
that of congeners not subjected to drought (Marsh-Matthews and Matthews 2010). Orangethroat darters that survived an experimental drought showed substantial postdrought recovery of physical condition (Marsh-Matthews
and Matthews 2010), and this species showed large population increases in Brier Creek in 1999 and 2000 after the
two most severe droughts, with the most young-of-year
darters we have ever observed in the system.
There was also a major increase in numbers of youngof-year largemouth bass in 1999 and 2001, and a dramatic
increase in young suckers in 2001 after the second extreme
drought. The mechanisms underlying these reproductive
bursts are not known, but the suckers are large-bodied,
highly mobile species that might lack suitable refugia in
Brier Creek during extreme drought, and adults might have
migrated downstream to permanent water in or near the
reservoir. Adult suckers migrate upstream to spawn, and
might have done so in 2001, following the 2000 drought.
One possible mechanism that could have enhanced reproduction by the suckers as well as bass is that several
insectivorous minnow species that also eat fish eggs or
larvae were not detected in 1999 and were very scarce in
2001. The sharp decline in minnows also coincided with
long-term increases in abundance of their potential predators (large sunfish and black bass), shown to have important effects on minnows in this system by Power and
Matthews (1983) and Marsh-Matthews et al. (2011). Red
shiners, blacktail shiners, and sand shiners all eat fish eggs
(Surat 1979), and red shiners are aggressive predators of
Oecologia
sucker larvae (Karp and Tyus 1990) or other species (Gido
et al. 1999). So, for the benthic spawning species suckers
and bass, there might have been less predation pressure on
developing eggs or larvae in the years following the
droughts, when most minnows were absent or in very low
numbers. However, in the long view of the community, the
sharp peaks in suckers and bass due to increased production of young in the years after the 1998 or 2000 droughts
were not sustained, and did not result in a permanent elevation in abundance of these species after 2001.
The scenario above underscores the potential importance of the integration of biotic and abiotic factors and
interspecific interactions. We consider long-term increases
in piscivores in Brier Creek to be related to physical
changes in the environments lower in the creek (Matthews
and Marsh-Matthews 2007). If minnows declined due to
increases in predators, the effects of drought, or both, and
thus released gravel-spawning larger species (bass, suckers) from egg or larvae predation, resulting in better
recruitment of the latter, this complex array of interactions
of physical structure, drought-related stress, and species
interactions, would be worthy of more experimentation or
species-specific, trait-based modeling, in Brier Creek or
other systems.
We suspect that mechanisms related to individual species
traits, such as high tolerance for thermal or oxygen stress
(Matthews 1987), ability to survive during or recover from
drought-related stresses (Marsh-Matthews and Matthews
2010), or seek out refuge habitats during flood or drought
and then recolonize (Matthews 1987), all help to produce
long-term stability in the community under the current climate and disturbance regime. We do know that the species
best surviving drought in Brier Creek the early 1980s, and
most successfully recolonizing and producing young in rewatered headwater reaches, were species with the greatest
tolerance for low oxygen conditions (Matthews 1987).
Conclusion
Our findings suggest that the Brier Creek community since
1969 had tended toward deterministic regulation about a
loosely stable (Collins 2000) equilibrium, with generally
persistent (Bêche and Resh 2007) core species, little species
turnover, and species abundances that tend to return toward
average (Bêche and Resh 2007; Magurran and Henderson
2010) in spite of the transient impacts of some events. In
recent evolutionary time the fish community in the dynamic
environment of Brier Creek has been exposed to frequent
disturbances or harsh physical conditions, and individual fish
species are well adapted to cope with vicissitudes typical of
the past (Matthews 1987). But if predictions about global
climate change, and increased frequency of severe events
(Sheffield et al. 2012) are correct, then they, and many other
animal and plant communities, will in the future be subject to
repeated, frequent episodes outside the range of previous
evolutionary experience. From a conservation perspective,
predictions indicate that the southwestern United States will
become hotter and drier, with droughts more frequent and
more severe (US Global Change Research Program;
http://www.globalchange.gov). In other habitats like coastal
regions, storms like hurricanes may become more severe or
more frequent. Geheber and Piller (2012) clearly show in a
22-year data set the strong alteration of a community after
hurricanes Katrina and Rita, only a month apart in 2005. To
the extent that the response of the Brier Creek community to
consecutive severe droughts also serves as a model, there
should be concern that the future climate could push systems
beyond limits from which even naturally hardy native
communities may not recover (Matthews and Zimmerman
1990). Being attuned to the fact that sequences of events, like
the repeated severe droughts in Brier Creek, may have synergistic effects that are more than a ‘‘sum of the parts,’’ may
provide a stimulus to and focus for future field, experimental,
or modeling studies of all kinds of aquatic and terrestrial
communities.
Acknowledgments We thank two anonymous reviewers and the
editors for helpful suggestions that improved the manuscript. We
thank C. L. Smith for his seminal research and for sharing data,
A. Echelle for leading the 1976 survey, S. T. Ross for detailed
analyses of surveys through 1981, and K. Hauger, C. Hargrave,
A. Marsh, R. Marsh, S. M. Matthews, C. Deen, M. Walvoord,
I. Camargo, M. Brooks, N. Franssen, J. Stewart, and P. Lienesch, and
students at the University of Oklahoma Biological Station classes for
assistance in the field. We thank J. F. Schaefer for consulting on use of
the Monte Carlo simulation program. We thank the University of
Oklahoma Biological Station and the Department of Zoology for
logistical or financial support, and the US Environmental Protection
Agency for funding to W. J. M. and E. M. M. for some surveys. We
thank all Brier Creek landowners upon whom this research depends,
including J. Martin, J. Woody, R. Coleman, and J. Williams. All fish
collections were made with permits from the Oklahoma Department of
Wildlife Conservation, and, in recent decades, with Institutional Animal
Care and Use Committee permits from the University of Oklahoma.
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