J. N. Am. Benthol. Soc., 1997, 16(2):425-438
? 1997 by The North American Benthological Society
Exploring how disturbance is transmitted upstream:
going against the flow
CATHERINEM. PRINGLE
Institute of Ecology, University of Georgia,Athens, Georgia30602 USA
Abstract. Modifications of lower watersheds such as water abstraction, channel modification, landuse changes, nutrient enrichment, and toxic discharge can set off a cascade of events upstream that
are often overlooked. This oversight is of particular concern since most rivers are altered by humans
in their lower drainages and most published ecological investigations of lotic systems have focused
on headwater streams. Factors contributing to ecological processes or biophysical legacies in upper
watersheds often go unacknowledged because they occur at disparate geographic locations downstream (e.g., gravel mining, water abstraction, dams) with significant lag times.
This paper considers examples of how alterations to streams and rivers in their lower reaches can
produce biophysical legacies in upstream reaches on levels from genes to ecosystems. Examples
include: 1) genetic- and species-level changes, such as reduced genetic flow and variation in isolated
upstream populations; 2) population- and community-level changes that occur when degraded downstream areas act as population "sinks" for "source" populations of native species upstream or, conversely, as "source" populations of exotic species that migrate upstream; and 3) ecosystem- and
landscape-level changes (e.g., nutrient cycling, primary productivity, regional patterns of biodiversity)
that can occur in headwater systems as a result of downstream habitat deterioration and hydrologic
modifications.
Finally, a case study from my own research illustrates the importance of careful consideration of
downstream-upstream linkages in formulating research questions, designing experiments, making
predictions, and interpreting results. The effects of dams and associated water abstraction in lowland
streams of Puerto Rico has forced my colleagues and me to re-evaluate the results of ecological
research that we have conducted in highland streams over the past decade and to redirect our research to consider downstream-upstream linkages.
Key uords: biophysical legacies, streams, rivers, downstream-upstream linkages, exotic species,
hydrologic and geomorphic change, migratory species, human disturbance.
Despite our increasing conceptual understanding of stream connectivity (e.g., Ward and
Stanford 1989), downstream influences on upstream communities remain little explored. The
River Continuum Concept and other lotic paradigms emphasize that downstream communities are a function of upstream processes (e.g.,
Vannote et al. 1980, Newbold et al. 1981, Minshall et al. 1985). While it is acknowledged that
upstream transfers may occur (e.g., migration of
fishes [Hall 1972] and adult insects with larval
aquatic stages [Hershey et al. 1993, Anholt
1995]), the extent to which upstream communities are a function of downstream processes
has not been a major focus, most likely as a result of the historical and logical emphasis on a
unidirectional flow of current and energy. Accordingly, while many studies have focused on
the downstream effects of human disturbance
(e.g., Holden 1979, Mason 1991), very few have
examined how human activities downstream
affect communities and processes upstream (but
see Winston et al. 1991, Osborne and Wiley
1992, Hartfield 1993).
Given that most published studies deal with
low-order or headwater streams (Hynes 1989),
it is crucial that aquatic ecologists develop an
understanding of the role of downstream impacts in determining biophysical legacies upstream. When disturbances that have played a
major role in determining the current biophysical state or legacy within a stream reach have
occurred in a different geographic area from the
site under study, it is difficult to determine their
if they occurred downroles-particularly
stream with a significant lag time between
cause and effect.
Legacies have been defined as the remnants
or "signatures" of past biological and physical
disturbances (Naiman et al. 1995). In freshwater
systems, legacies comprise the present habitat
and biota resulting from past events such as glaciation, floods, and severe anoxia (Naiman et al.
1995). Legacies are receiving increasing recog-
425
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C. M. PRINGLE
426
nition from aquatic ecologists as important measures of environmental conditions that build the
foundation for freshwater ecosystem management. A workshop group on legacies, which was
convened as part of the "Freshwater Imperative" initiative, identified 3 key research needs:
1) identification of the origins and historical spatio-temporal development of past, present, and
future legacies; 2) understanding the role of legacies in ecosystem function; and 3) understanding current and projected patterns of legacy development (Naiman et al. 1995).
This paper examines how downstream influences can affect upstream structure and function, specifically addressing: 1) how human alterations in the lower reaches of streams produce biophysical legacies in upstream reaches at
different scales, from genes to ecosystems to
landscapes (Fig. 1); 2) the management implications of these downstream-upstream connections; and finally 3) a case study from my research in Puerto Rico which illustrates the importance of carefully considering downstreamupstream linkages in formulating research
questions, designing experiments, making predictions, and interpreting results.
Effects of human activities in lower
watersheds on upstream communities
Genetic-and species-levelchanges
As stream systems become increasingly fragmented along their longitudinal continua by human impacts, upstream populations of aquatic
biota are subject to reduced genetic flow and
variation (Fig. 1). Moyle and Williams (1990)
noted that while fish assemblages found at middle to high elevations in streams in California
might be intact, the disruption of lowland habitats isolated fish populations in different tributary drainages. As pointed out by Meffe
(1987), while a species either exists or it does
not, decreases in intraspecific genetic diversity
are inconspicuous and thus easily overlooked.
Furthermore, we know very little about conserving genetic diversity in aquatic systems (Vrijenhoek et al. 1985, Meffe 1987).
The Cherokee darter, Etheostoma scotti, provides an example. This species is endemic to
portions of the Etowah River System in the
Piedmont region of Georgia, USA. Because of
the isolated range of E. scotti, which is frag-
[Volume 16
mented by degraded habitat (urbanization and
different types of human land-use), there is no
potential genetic exchange between populations
(B. J. Freeman, University of Georgia, personal
communication). For obligate riverine species
with large home ranges, impoundments may
similarly fragment the range, causing loss in genetic diversity and local extinctions (Winston et
al. 1991).
It is useful to compare the process of genetic
isolation caused by human-induced fragmentation of stream continua with "natural" fragmentation and isolation processes. For instance,
natural desert stream systems in North America
are fragmented on both broad geographic and
local scales. Many taxa are relicts that have been
trapped in isolated springs and streams during
the past 10,000-12,000 years, resulting in a high
degree of endemism (Williams et al. 1985). The
consequences of this fragmented distribution
may include little or no gene flow among isolated demes and little or no recolonization of
isolated habitats after local extinction. Fishes of
southwestern USA are thus naturally "extinction prone" and are exceedingly vulnerable to
habitat destruction and the introduction of exotic species. An important distinction here is
that the natural fragmentation of stream systems in the southwestern US occurred over geological time. In contrast, the human-induced
fragmentation processes that are altering stream
continua today are occurring rapidly over a period of years, often exceeding the limits of developmental plasticity and resulting in extinction.
The genetic- and species-level effects of dams
on economically important migratory fishes,
such as anadromous salmonids, have received
much attention (Mills 1989, Nehlsen et al. 1991,
Meffe 1992). Over 100 major salmon and steelhead populations or stocks are known to have
been extirpated on the west coast of the US and
Canada, while an additional 214 face a moderate to high risk of extinction or are of special
concern (Nehlsen et al. 1991). In North America,
even less is known about genetic- and specieslevel effects of stream fragmentation on stream
biota of less economic importance (e.g., other
fish taxa, freshwater shrimps). In tropical areas
such as the Amazon, fish migratory patterns are
so complex-covering huge drainage areasthat the direct effects of dams and other forms
of stream fragmentation are unknown for even
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1997]
UPSTREAMLEGACIESOF DOWNSTREAMDISTURBANCE
427
Upstream
biological legacies
- Genetic Isolation
Population-levelchanges
'Source' of native species
'Sink'for exotic species
* Ecosystem-level changes
Primaryproduction
Nutrientcycling
Decomposition
Downstream
humanactivities
Urbanization
Dams and impoundments
*Gravel mining
*
Channelization
FIG. 1. Potentialdownstreaminfluenceson upstreamcommunities.
economically important fish species (e.g.,
Goulding et al. 1996).
semblage structure with heavy metal and pes-
and community-level
Populationchanges
for populations of native fishes. Furthermore,
only those fishes most tolerant of degraded en-
Degraded downstream areas can potentially
act as population "sinks" (e.g., Pulliam 1988,
Pulliam and Danielson 1991, Woottonand Bell
1992) for native riverine species and, alternatively, as "sources"of exotic species or facultative riverinespecies (Fig. 1).
For instance, in his studies of streams draining urban areas in the Apalachicola-Chattahoochee-Flint RiverBasin (Georgia),DeVivo (1996)
found highly variable fish faunas, atypical age
structures, and a correlation between fish as-
ticide levels. He suggested that less-disturbed
sites within the system might be acting as sinks
vironmental conditions (often exotic species)
had well-establishedpopulations.
Consequently, stream reaches that are upstream of degraded downstream areas are vulnerableto exotic species that are often common
in degraded areas.Such degraded areascan potentially act as "source" populations of exotic
species. For example, the red shiner (Cyprinella
lutrensis)is a cyprinid that is native to the Mississippi River drainage. Although its sale as a
bait fish for sport fishing is now illegal in the
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428
C. M. PRINGLE
state of Georgia, in 1978 small numbers of C.
lutrensis were observed in the ApalachicolaChattahoochee-Flint River system, presumably
introduced as a discarded "bait bucket" species
(DeVivo 1995). The species has since gained a
strong foothold in degraded streams around Atlanta (which are characterized by high turbidity,
extremes of discharge and temperature, and
high nutrient levels), becoming dominant or codominant at the expense of native species and
often accounting for up to 90% of the fish populations (DeVivo 1995). Its success is apparently
due to competitive exclusion of native fishes in
degraded systems and possibly to its tendency
for hybridization with native congenerics. Reproducing populations of C. lutrensis will most
likely remain intact as long as in-stream habitat
remains degraded (DeVivo 1996 and references
therein).
With the proliferation of dams and associated
impoundments, headwater streams are also becoming increasingly vulnerable to invasion by
facultative riverine species that become established in reservoirs. For example, species such
as the gizzard shad Dorosoma cepedianum and
the common carp Cyprinus carpio proliferate in
impoundments and then move upstream in
large numbers, potentially competitively displacing populations of obligate riverine species
and causing major changes in the ecosystem
(Erman 1973). Similarly, Winston et al. (1991)
found that 4 minnow species were extirpated in
the North Fork, a prairie stream in southwestern
Oklahoma, following damming. Upstream of
the reservoir, the sand shiner (Notropis stramineus) and the emerald shiner (N. atherinoides)replaced the plains minnow (Hybognanthusplacitus) and the Red River shiner (N. bairdi)as predominant species. In addition, both the speckled chub (Macrhybobsisaestivalis) and the chub
shiner (Notropis potteri) were extirpated upstream. Several possibilities were suggested to
account for the collapse of these populations
(Winston et al. 1991): 1) as the North Fork began
to dry up in late summer the riverine species
were forced to move into the reservoir where
they were poorly adapted to lentic conditions
and easy prey for large piscivorous fish; 2) the
reservoir may have provided a base from which
piscivorous fishes could move upstream, preying upon the declining species; 3) the speckled
chub and plains minnow spawn semi-buoyant
eggs during high water, and the embryos or lar-
[Volume 16
vae of these species could have been washed
into the reservoir where they failed to survive;
4) prolonged drought could have caused spawning failures and loss of entire year-classes; and
finally 5) fish populations now extirpated in the
upper river might not have spawned there before damming and may only have occurred
there as a result of dispersal from downstream
spawning sites. This study clearly illustrates the
importance of examining upstream effects of
dams and impoundments and how little we
know about possible mechanisms by which
these effects can be transmitted.
There is also increasing evidence that small
natural barriers and associated impoundments
(e.g., those created by beaver [Castorcanadensis])
along stream continua can affect the composition of fish assemblages in upstream reaches.
Schlosser (1995) presented evidence suggesting
that beaver impoundments along streams act as
reproductive "sources" for fishes in the landscape, while adjacent stream environments act
as potential "sinks." Osborne and Wiley (1992)
illustrated upstream-downstream gradients in
immigration rates of warmwater fish assemblages, from low-immigration headwaters to
high-immigration downstream reaches. Snodgrass (1996) found that stream impoundment by
beavers increased species diversity as much as
2-fold in headwater streams and this effect was
highly dependent on pond age. His data also
suggest that large scale (drainage basin) patterns of fish species diversity were probably altered by the reduction of beavers in many
streams in the USA at the turn of the century.
Dams are obvious examples of human activities that block the migration of aquatic organisms. Effects of other types of "selective environmental filters" (see Poff 1997) are much less
obvious and they may or may not be associated
with dams; they include flood frequency,
drought frequency, pollution level, thermal
stress, and hydrologic modifications such as
headward erosion or "headcutting" (Hartfield
1993). Removal of gravel and sand from the
streambed can initiate extensive erosion
throughout the system and headcutting is the
upstream progression of such erosion (Smith
and Patrick 1991, Patrick et al. 1991, 1993, Mount
1995). Headcutting occurs because the channel
slope increases (as a result of hydrological modification), with an inflection point or "knickpoint" at the upstream end of the disturbed
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1997]
UPSTREAM LEGACIES OF DOWNSTREAM DISTURBANCE
reach. The increased current velocity associated
with the increased channel slope results in erosion along the affected reach, which becomes
concentrated at the knickpoint. The knickpoint
may be removed by erosion and channel deepening and these processes can extend many
miles upstream (Patrick et al. 1993), with population- and community-level consequences.
For example, Hartfield (1993) documents the
negative effects of headcutting on populations
of several endangered mussel species. Being relatively immobile, mussels are particularly vulnerable to channel degradation and sedimentation processes associated with headcutting.
Another example concerns the bayou darter
(Etheostoma rubrum), which is endemic to the
Bayou Pierre River system in Mississipi. The
middle and upper reaches of the Bayou Pierre
River have suffered stream bank erosion as a
result of hydrologic modifications downstream
(Patrick et al. 1991). The rate of knickpoint
movement increased from 46 m/y between 1940
and 1964, to 124 m/y between 1964 and 1978,
and to 222 m/y between 1978 and 1985. Channel width increased from 30 to 57 m in some
portions of the river between 1940 and 1985.
The bayou darter occurs in stable gravel beds in
shallow riffles, and its upstream distribution is
largely defined by the uppermost locations of
knickpoints in the Bayou Pierre and its major
tributaries. Populations of E. rubrum have
tracked the upstream movement of the knickpoint where they colonize preferred riffle habitats. Correspondingly, populations of this species are diminishing in lower stream reaches as
a result of sedimentation from upstream erosion
(Patrick et al. 1991).
Ecosystem- and landscape-levelchanges
When major faunal components of an ecosystem are excluded from upper portions of the
watershed as a result of human activities downstream, a cascade of ecosystem-level effects may
occur, particularly when the extirpated component was an important food source, predator,
host species, or habitat modifier (Fig. 1). For instance, populations of bald eagles and other animals that depend on migrating salmon as food
may decrease dramatically if this food is eliminated (e.g., Spencer et al. 1991). Also, because
most unionid mussels require a fish host for
their parasitic glochidial stage, loss of migratory
429
host fish taxa can result in decline or extinction
of mussels.
The past ecological roles of many migratory
organisms and their potential ecosystem- and
landscape-leveleffects are easily overlookedbecause these migrants no longer enter upstream
reaches.Of the 5.1 million km of streams in the
lower 48 states of the US, only 2%are free-flowing and relatively undeveloped; the remaining
98%have been alteredby dams, waterdiversion
projects,etc (Benke1990).Only 42 free-flowing
rivers > 200 km long now exist.
Faunal components now absent could have
played key roles in ecosystem-level properties
and processes such as water quality and nutrient cycling. For instance, salmon remove fine
particulate organic matter in bed sediments
during spawning (R. J. Naiman, University of
Washington, personal communication). They
also release nutrients when they die after
spawning, affecting algal biomass and primary
production (e.g., Richey et al. 1975, Kline et al.
1990) and secondary insect consumers (Schuldt
and Hershey1995).The releaseof nutrientsfrom
decomposing salmon is consideredessential for
maintaining the productivity of nursery areas
for future stocks of salmon (Mathisen 1972).
Consequently,when dams block salmonid migrationroutes,patternsof nutrientcycling in entire stream ecosystems can potentially be altered.
Although some attentionhas been paid to the
biophysicallegacies in streamsystems resulting
from the loss of salmonids, the ecological and
ecosystem-leveleffects of many extirpatedbiota
are not known. Forexample, 16 impoundments
along the mainstem Chattahoocheeand Flint
rivers in Georgia alter the natural hydrologic,
temperature,and nutrientregimes downstream
and prevent the spawning migrationsof 8 species of anadromous and catadromous fishes
(DeVivo 1996).Three of the fish species, Acipenser oxyrhynchus,
Alosaalabamae,
and Agonostomus
monticola,are listed for either federal or state
protection (DeVivo 1996). What are the biophysical legacies in the Chattahoocheeand Flint
watershedsresulting from the loss or decline of
these fish species? How have ecosystem-level
processes been altered?
Otherecosystem-levelchanges resultingfrom
dams are just being elucidated.An example is
the relativelyrecent discovery that mercurycan
be a by-productof reservoirformationbecause
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430
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C. M. PRINGLE
of high rates of conversion of inorganic mercury
to methylmercury in the flooded sediments of
new impoundments (Hecky et al. 1991). Mercury in fish can attain very high levels in reservoirs, sometimes exceeding the marketing
limit (see review by Rosenberg et al. 1995). Although studies have documented that significant levels of mercury can be expected in fishes
many km downstream from reservoirs (Rosenberg et al. 1995), research is necessary to ascertain if, and to what extent, bioaccumulation effects extend upstream.
As discussed previously, hydrologic modifications in specific rivers have been documented
to have biophysical consequences within upstream reaches through headward erosion
(Hartfield 1993, Mount 1995). However, effects
of hydrological modifications (e.g., gravel mining) in lowland streams on landscapepatterns in
biota and ecosystem-levelprocesses remain virtually unexplored by lotic ecologists. This is a major cause of concern, given the magnitude and
extent of hydrologic modifications and headward erosion. For example, in California alone,
>900 companies are involved in the extraction
and processing of aggregates (e.g., sand and
gravel deposits) from stream channels, floodplains, and terraces throughout the state. Over
the past 10 y, >109 tons have been removed,
probably representing as much as 10x the
amount of bedload supplied to rivers by the state's watersheds, essentially resulting in sediment-starved rivers (Mount 1995 and references
therein). On a regional scale, the decline of sediment yields has led to widespread incision,
bank erosion, and loss of gravel bards. The incision lowers local groundwater tables, and
bank erosion reduces riparian cover, often destroying bridges and other structures upstream
of mining operations (Mount 1995 and references therein).
One reason for our lack of knowledge of the
consequences of downstream hydrologic modifications on upstream conditions is the lag time
between cause and effect: channel erosional
stresses are greater during flood stages, and
changes resulting from gravel mining and channelization usually appear following seasonal
flood periods and are often erroneously attributed to local erosion from natural causes (Hartfield 1993).
The upstream effects of groundwater exploitation in lower stream drainages also have been
largely overlooked. The increasing exploitation
of groundwater reserves for municipal, industrial, and agricultural use is having profound
effects on riverine ecosystems, as groundwater
tables are lowered. For example, populations of
the anadromous striped bass (Morone saxatilis)
are dependent on cold-water refuges within riverine systems during hot summer periods because of their high oxygen requirement (Coutant 1985). As a result, populations of striped
bass are healthy and productive in stream systems of southeastern USA that have a high thermal diversity where they can search out and use
spring-fed areas as refuges (e.g., Van Den Avyle
and Evans 1990). Studies using radio telemetry
to track striped bass distributions in the Apalachicola River system in Georgia showed that
fishes were moving into isolated springs when
the ambient river temperature neared their upper avoidance temperature (Van Den Avyle and
Evans 1990). Extensive groundwater withdrawals are threatening these springs and the survival of biota dependent on cold water refuges,
thus having the potential to affect regional patterns of biodiversity.
Management implications of
downstream-upstream effects
An understanding of environmental disturbances in lower watersheds and how they are
transmitted upstream, associated lag times, and
resultant upstream legacies has important management implications. The concept of downstream-upstream linkages can be incorporated
into watershed management plans to protect
stream ecosystems.
On genetic and species levels, it is important
to locate and protect systems that are acting as
source populations for native fishes (Howe et al.
1991). Natural isolated populations of fishes in
upstream reaches should be identified, genetically analyzed, and monitored (e.g., Vrijenhoek
et al. 1985, Meffe 1987). We should develop our
knowledge of "source-sink" population dynamics as a management tool for aquatic systems. Despite the presence of apparently
healthy populations in upstream areas, we
should not assume that we have a "natural" situation (e.g., degraded downstream areas may
be acting as a potential "sink" for native species
or as a "source" of exotics or facultative riverine
species that have become established in im-
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19971
UPSTREAMLEGACIESOF DOWNSTREAMDISTURBANCE
poundments). Wherever possible, it is important
to mitigate effects of downstream degradation
through habitat improvement/restoration.
In a landscape exposed to increasing levels of
fragmentation, the use of dams to manage upstream populations of native fishes may become
an important management strategy. Until the
last few decades, dams and reservoirs in the
western US were often viewed as opportunities
to introduce game fishes; managing for native
nongame fishes was unheard of. For example, in
1962 the Wyoming and Utah Fish and Game
Departments poisoned 715 km of the upper
Green River with rotenone to remove local
"trash" fishes (mostly native cyprinids and catostomids) from the newly created Flaming
Gorge Reservoir to allow planted salmonids to
become established (Holden 1991). Remnant upstream populations of native fishes that are now
extremely rare (e.g., bonytails [Gila elegans] and
the razorback sucker [Xyrauchen texanus]) did
not persist in the river or reservoir above the
dam. Today, remnant populations of bonytails
and razorback suckers from other drainages are
providing brood strocks for recovery of these
endangered species (Holden 1991).
More recently, dams are being used to protect
native species in upstream reaches by preventing the upstream migration of harmful exotics.
For example, the native greenback cutthroat
trout (Oncorhynchusclarkistomias) is 1 of 4 native
species of cutthroat trout found in Colorado in
the 1800s. It is smaller than other trout species
and more vulnerable to displacement by varieties that were introduced throughout most of
the western US. Introduced juvenile brook trout
(Salvelinusfontinalis) are particularly aggressive,
displacing juvenile greenbacks from sheltered
backwaters into the main channel and making
them vulnerable to predation (Middleton and
Liittschwager 1994). Adult rainbow trout often
breed with greenbacks and produce hybrids.
The greenback cutthroat trout was one of the
first species to be listed as endangered in 1973
when the US Endangered Species Act was
passed. Since the cutthroat trout was listed,
managers have systematically removed brook
trout from 2 river systems where remaining cutthroat populations survived. The cutthroat trout
has partially recovered and its status was upgraded to threatened in 1978. Permanent physical barriers must be maintained to insure that
431
non-native species do not return (Middleton
and Liittschwager 1994).
Hydrologic changes in lower watersheds that
affect upstream ecosystems and landscape patterns should be identified and mitigated. Although high rates of headward erosion exacerbated by human activities have been increasingly documented in the southeastern US (e.g., Patrick et al. 1991, Hartfield 1993) and California
(Mount 1995), the extent and effect of headward
erosion in other regions needs to be investigated. Specific recommendations provided by Patrick et al. (1991) include: 1) sand and gravel
mining in and along the stream channel and on
the flood plain should be either eliminated altogether or regulated more strictly through the
permitting process in order to control stream
sedimentation; 2) vegetated buffer zones should
be established and maintained along the sides
of stream channels to stabilize banks and minimize streambank erosion; and lastly 3) we
should develop an understanding of headcutting and its biological consequences (e.g., what
are the changes in relative population sizes of
aquatic biota above and below active erosional
areas including knickpoints).
Also, regional planners and developers
should consider the influence of groundwater
withdrawals on riverine habitat (e.g., cold-water
springs which are used by striped bass as a
thermal refuge). Biologists and hydrologists
need to become involved in determining "sustainable" watertable heights for stream systems.
Case study: Ecological studies in highland
streams draining the Caribbean
National Forest, Puerto Rico
Here I explore a case study from my own research program, in montane streams draining
Puerto Rico's Caribbean National Forest, as an
example of the importance of considering
downstream-upstream connections in formulating research questions, designing experiments,
making predictions, and interpreting results.
The Caribbean National Forest (CNF) is in the
highlands of northeastern Puerto Rico (Fig. 2)
and is the largest natural forest (11,269 ha) left
in the Caribbean islands. The CNF is also a major site for tropical research. It was declared a
Biosphere Reserve by the Man and the Biosphere Programme of UNESCO in 1976 and is
a site for Long Term Ecological Research
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432
[Volume 16
C. M. PRINGLE
San Juan
N
Key: Amphidromous :
Catadromous
[
FIG.3. The food web of highlandmontanestreams
in Puerto Rico indicating migratoryorganisms that
are vulnerableto water abstractionin lowland stream
reaches.Amphidromousand catadromousorganisms
both spend some part of theirlife cycle in the estuary/
ocean.
LuquilloExperimentalForest boundary
Watershedboundary
I
1 km
FIG.2. Locationof the CaribbeanNationalForest
in northeastemPuertoRico,showing the 9 majorriver
drainagesof the forest,all of them dammedexceptfor
the MameyesRiver.
(LTER), as designated by the US National Science Foundation. One of the goals of current
LTER research is to assess the effects of disturbances on ecosystem function. The occurrence
of Hurricane Hugo in 1989, soon after the initiation of the LTER program, has provided an
opportunity to study long-term ecosystem dynamics in response to natural disturbance.
Streams draining the CNF are characterized
by a simple food chain typical of oceanic islands
(Fig. 3). The macrobiota of some tributaries
where predaceous fishes are absent (due to
large waterfalls downstream) is dominated by
large numbers of freshwater atyid shrimps (i.e.,
Atya and Xiphocaris spp.) (Covich 1988, Pringle
et al. 1993, E. Garcia, US Forest Service, personal
communication). In other streams, where pre-
daceous fishes-Agonostomus monticola (Bancroft), Auous tajasica(Lichtenstein), and Anguilla rostrata (LeSeur)-are present, freshwater
atyid shrimps are often much less abundant
(Pringle 1996).
Almost all of the stream macrobiota in highland streams must spend some part of their life
in the estuary/ocean to complete their life cycle
(Fig. 3). The migration of these organisms forms
a dynamic linkage between stream headwaters
and their estuaries. In the case of amphidromous shrimps and 2 fish species (A. tajasica and
Sicydium plumier), newly hatched larvae migrate
downstream and complete their larval stage in
the estuary. Upon metamorphosis, the juveniles
migrate upstream where they live as adults. The
2 catadromous fishes (i.e., A. monticola and A.
rostrata)spend most of their lives in freshwater,
but migrate to the sea to breed (Fig. 3).
Basic research in streams dominated by atyid
shrimps has shown that these relatively large
invertebrates can have a dramatic effect on sedimentation, insects, algal standing crop, and
community structure (e.g., Pringle et al. 1993,
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433
UPSTREAM LEGACIES OF DOWNSTREAM DISTURBANCE
1997]
0.1mm
W
(b)
FIG. 4. Schematic diagram illustrating interstream differences in primary producers in (a) a stream characterized by high densities of atyid shrimp with no predaceous fishes, and (b) a stream with very low numbers
of atyids and characterized by the presence of predaceous fishes. The atyid-dominated stream (a) had bluegreen algal bands in shallow (< 3 cm) pool margins where atyids did not forage; in deeper water, atyids
maintained a low-growing understory turf dominated by sessile diatoms (Bacillariophyta) and sometimes closely cropped filamentous blue-green (Cyanophyta) algae. In the atyid-poor stream (b), algal assemblages were
characterized by high standing crop of loosely attached epipelic diatoms and no depth zonation.
Pringle and Blake 1994, Pringle 1996). Lower algal standing crop and distinctly different algal
community assemblages were found in an
atyid-dominated versus an atyid-poor stream
(Fig. 4). Inter-stream rock and shrimp transplant experiments showed that atyid shrimps
significantly reduced algal standing crop and
altered algal assemblage composition, supporting the hypothesis that they play a major role
in determining observed interstream differences
in algal communities in the highlands (Pringle
1996).
A working hypothesis is that in the headwaters of the Rio Espiritu Santo (Fig. 2; 1 of the 9
major streams draining the CNF), abundant
atyid shrimps are one of the upstream legacies
of a -12-m-high waterfall located at -200 m
a.s.l. The waterfall is easily negotiated by
shrimps but not by predaceous fishes (personal
observation). Other potential upstream legacies
of this geomorphic barrier include reduced algal
standing crop and sediment cover, and changes
in algal assemblage composition (Fig. 5), which
are associated with abundant atyid shrimps
(Pringle et al. 1993, Pringle and Blake 1994,
Pringle 1996).
A major factor that we haven't adequately
considered in our basic research is the impact
of dams and associated water abstraction from
lower stream reaches on faunal composition and
related ecosystem processes in highland
streams. In 1994, a water budget was developed
for the CNF (Naumann 1994). This budget
shows that 21 water intakes are operating within the CNF and 9 large intakes outside the forest, resulting in significant stream dewatering.
On an averageday,over50% of riverinewaterdraining the forest is diverted into municipal water sup-
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All use subject to JSTOR Terms and Conditions
C. M. PRINGLE
434
I
[Volume 16
Upstream legacy
of waterfall
Range of predatory
fishes
* No predatoryfishes
* Abundantatyidshrimps
* Lowalgal standingcrop
x Reducedsediment cover
r
WATE RFALL
Upstream legacy of dam
and water abstraction
* Reduced recruitmentof
juvenileshrimps?
* Skewed age distribution
of shrimps?
---
'Natural'
* Hurricanes
* Droughts
DAMAND WATER
ABSTRACTION
Human
* Poisoningof streamreaches
* Shrimp trapping
* Fishing
* Sewage effects
FIG.5. Schematic diagram of the Rio Espiritu Santo, Puerto Rico, illustrating observed and potential downstream-upstream effects. Barriers, both natural (waterfalls) and artificial (dams and associated water abstrac-
tion), act as selective filters along the stream continuum.Superimposedon the upstream legacies createdby
these filters are the legacies created by interactiveeffects of both natural (e.g., hurricanesand droughts)and
artificial(streampoisoning events, fishing, shrimp trapping,pollution)disturbances.
plies (via zwterintakes)beforeit reachesthe ocean. niles returning from the estuary. Studies conSeveralrivershaveno waterbelowthesewaterintakes ducted during 1995 (J. P. Benstead, University
of Georgia, personal communication)indicated
for muchof theyear.
Given this information, my graduate students
that water abstractionassociatedwith a dam in
and I have redirected our basic research to eval- the lower stretches of a main river drainage
uate how dams and associated water withdrawals affect the downstream migration of larval
shrimps and the upstream recruitmentof juve-
within the CNF (Rio Espiritu Santo; Fig. 2) sig-
nificantly affects shrimp recruitment,causing
direct mortalityof over 50%of migratinglarvae
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All use subject to JSTOR Terms and Conditions
1997]
UPSTREAM LEGACIES OF DOWNSTREAM DISTURBANCE
which are entrained into water intakes for municipal water supplies. During drought periods of
low flow, no water is discharged over the dam, all
migratoryshrimp larvae are killed, and saltwaterintrudes severalkm inland to the base of the dam. Although the dam at the water intake does not
appear to be a barrier to the upstream migration
of returning juvenile shrimps, observations
show that it functions as a predation gauntlet
for juveniles due to the accumulation of both
freshwater and marine predaceous fishes below
the dam (J. P. Benstead, personal communication).
Effects of water abstraction are magnified
during drought years. Since 1992, rainfall in
Puerto Rico has been below average. In 1994, the
Commonwealth of Puerto Rico was declared an
agricultural disaster area by the US Federal
Government. Water rationing was imposed on
areas of the capital city, San Juan, for days at a
time, with serious negative effects on the economy. The pressure on the nearby CNF for water
supplies is increasing.
The most recent water demand studies predict that between the years 1990 and 2040, the
demand for water in the municipalities along
the northern border of the CNF (Fig. 2) will increase from 28.3 million gallons per day (MGD;
1.24 m3/s) to 36.1 MGD (1.58 m3/s) (US Army
Corps of Engineers 1993). Most of this increase
in demand will occur before the year 2000. At
present, all except 1 of the 9 stream drainages
within the CNF have dams and associated water
withdrawals on their main channels. A proposal
is currently being considered to dam the last
remaining undammed river, the Rio Mameyes
(Garcia 1994). The magnitude of current water
withdrawals from the CNF is already in conflict
with other important functions of the forest, including recreation, scientific research, and maintenance of the biointegrity of the island.
Consideration of downstream-upstream linkages (Fig. 5) has forced us to re-evaluate and
redirect the research that we have conducted in
the highlands of the Caribbean National Forest
over the last decade, and has stimulated the following questions:
1) What incorrect assumptions have we made
about our study site in the highlands that
need to be re-examined?
2) How "natural" are these stream systems?
3) To what extent are stream biota and associ-
435
ated ecological processes in highland
streams a legacy of water withdrawals (and
associated losses in shrimp and/or fish recruitment) in the lowlands?
4) How have aquatic communities in streams
draining Puerto Rico's Caribbean National
Forest been affected by the interaction of: a)
barriers along the stream continuum, both
natural (waterfalls) and artificial (dams and
associated water abstraction) and b) disturbances, both natural (hurricanes and
droughts) and artificial (stream poisoning
events, fishing and shrimp trapping, downstream pollution; Fig. 5)?
5) How can we predict patterns of ecosystem
function given the current and future massive water withdrawals that are planned for
streams of this region?
6) How can we apply our knowledge of downstream-upstream linkages to the development of management solutions to mitigate
the effects of water abstraction on stream
communities?
Conclusions and recommendations
This paper illustrates how alterations to
streams and rivers in their lower reaches can
produce effects in upstream reaches on levels
from genes to ecosystems. We make the following recommendations. First, our conceptual understanding of stream connectivity should be
expanded beyond traditional paradigms that
emphasize how downstream communities are a
function of upstream processes. Second, aquatic
ecologists should carefully consider effects of
downstream-upstream connections in formulating research questions, designing experiments,
and interpreting results: How do effects of natural and human disturbances in the lower watershed interact to affect the ecology of headwater streams (i.e., genetic- and species-level,
population- and community-level, and ecosystem- and landscape-level effects)? Finally,
resource managers should incorporate the concept of downstream-upstream linkages into
watershed management plans: How can downstream-upstream connections be manipulated
to protect riverine ecosystems?
Acknowledgements
I thank J Vaun McArthur for organizing the
symposium on "New Concepts in Stream Ecol-
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All use subject to JSTOR Terms and Conditions
C. M. PRINGLE
436
ogy" and the authorsof the papers included in
this volume for their stimulating insights and
ideas. I also thank R. J. Naiman,J.J. Magnuson,
and P. Firth for organizing the FreshwaterImperative Workshop and the members of the
"legacy"workshopin which I participated.Special thanks go to graduate students in my
course on "CurrentIssues in Aquatic Conservation" (1995) who provided valuable insights
and ideas, particularlyM. Hedrick and J. DeVivo, and to P. Hartfieldwho taught me about
headwarderosion.I am gratefulto R. J.Mackay
who provided invaluable editorial advice.
Thanks are also extended to T. Hamazaki for
preparationof figures and to J. Affolter,J. Benstead, T. Hamazaki, J. Karr,J. March, and A.
Ramirezfor their commentsand suggestions on
an earlierversionof the paper.I thankE Scatena
and the USDA ForestServicefor supportingmy
research activities and those of my graduate
students. The writing of this paper was supported in part by National Science Foundation
grant DEB95-28434.
Literature Cited
ANHOLT,B. R. 1995. Density dependence resolves the
stream drift paradox. Ecology 76:2235-2239.
BENKE,A. C. 1990. A perspective on America's vanishing streams. Journal of the North American
Benthological Society 9:77-88.
COUTANT,C. C. 1985. Striped bass, temperature, and
dissolved oxygen: a speculative for environmental risk. Transactions of the American Fisheries
Society 114:31-61.
COVICH,A. P. 1988. Atyid shrimp in the headwaters
of the Luquillo Mountains, Puerto Rico: filter
feeding in natural and artificial streams. Verhandlungen der Internationalen Vereinigung fur
theoretische und angewendte Limnologie 23:
2108-2113.
DEVIVO,J. C. 1995. Impact of introduced red shiners,
Cyprinellalutrensis, on stream fishes near Atlanta,
Georgia. Pages 95-98 in K. J. Hatcher (editor).
Proceedings of the 1995 Georgia Water Resources
Conference. Carl Vinson School of Government,
University of Georgia, Athens.
DEVIVO,J. C. 1996. Fish assemblages as indicators of
water quality within the Apalachicola-Chattahoochee-Flint (ACF) River Basin. Masters thesis. The
University of Georgia, Athens.
ERMAN, D. C. 1973. Upstream changes in fish populations following impoundment of Sagehen
Creek, California. Transactions of the American
Fisheries Society 102:626-629.
GARCIA,E. R. 1994. Proposed Mameyes dam/water
[Volume 16
withdrawal project: potential biological effects.
Internal report available from the U.S. Fish and
Wildlife Servce, Caribbean National Forest, Palmer, Puerto Rico.
GOULDING, M., N. J. H. SMITH, AND D. J. MAHAR. 1996.
Floods of fortune: ecology and economy along
the Amazon. Columbia University Press, New
York.
HALL, C. A. 1972. Migration and metabolism in a
temperate stream ecosystem. Ecology 53:585-604.
HARTFIELD, P. 1993. Headcuts and their effect on
freshwater mussels. Conservation and Management of Freshwater mussels. Pages 131-141 in
Proceedings of a conference on conservation and
management of freshwater mussels. Upper Mississippi River Conservation Committee, Rock Island, Illinois.
HECKY, R. E., D. J. RAMSEY, R. A. BODALY, AND N. E.
STRANGE.1991. Increased methylmercury contamination in fish in newly formed freshwater
reservoirs. Pages 33-52 in T. Suzuki, A. Imura,
and T. W. Clarkson (editors). Advances in mercury toxicology. Plenum Press, New York.
HERSHEY, A. E., J. PASTOR, B. J. PETERSON,AND G. W.
KLING. 1993. Stable isotopes resolve the drift
paradox for Baetis mayflies in an arctic river. Ecology 74:2315-2325.
HOLDEN, P B. 1979. Ecology of riverine fishes in regulated stream systems with emphasis on the Colorado River. Pages 57-74 in J. V. Ward and J. A.
Stanford (editors). The ecology of regulated
streams. Plenum Press, New York.
HOLDEN,P. B. 1991. Ghosts of the Green River: impacts of Green River poisoning on management
of native fishes. Pages 43-54 in W. L. Minckley
and J. E. Deacon (editors). Battle against extinction: native fish management in the American
West. University of Arizona Press, Tucson.
HOWE,R. W, G. J. DAVIS, AND V. MOSCA. 1991. The
demographic significance of 'sink' populations.
Biological Conservation 57:239-255.
HYNES,H. B. N. 1989. Keynote address. Pages 5-10
in D. P. Dodge (editor). Proceedings of the International Large River Symposium. Canadian Special Publication, Fisheries and Aquatic Sciences
106.
KLINE, T. C., J.J. GOERING, O. A. MATHISEN, AND P H.
POE. 1990. Recycling of elements transported upstream by runs of pacific salmon: 1. 15N and 13C
evidence in Sashin Creek, southeastern Alaska.
Canadian Journal of Fisheries and Aquatic Sciences 47:136-144.
MASON, C. F 1991. Biology of freshwater pollution.
John Wiley and Sons Inc., New York, 350 p.
MATHISEN, O. A. 1972. Biogenic enrichment of sockeye salmon lakes and stock productivity. Verhandlungen der Internationalen Vereinigung fur
This content downloaded from 128.192.10.126 on Wed, 3 Jul 2013 11:57:08 AM
All use subject to JSTOR Terms and Conditions
1997]
UPSTREAM LEGACIES OF DOWNSTREAM DISTURBANCE
437
values and management. National Association of
theoretische und angewandte Limnologie 18:
Conservation Districts, Washington, D.C.
1089-1095.
POFF,L. 1997. Landscape filters and species traits:
MEFFE,G. K. 1987. Conserving fish genomes: philostowards mechanistic understanding and predicophies and practices. Environmental Biology of
tion in stream ecology. Joural of the North
Fishes 18:3-9.
American Benthological Society 16:391-409.
MEFFE,G. K. 1992. Techno-arrogance and halfway
technologies: salmon hatcheries on the Pacific PRINGLE,C. M. 1996. Atyid shrimp (Decapoda: AtyiCoast of North America. Conservation Biology 6:
dae) influence spatial heterogeneity of algal communities over different scales in tropical montane
350-354.
streams, Puerto Rico. Freshwater Biology 35:1251994. WitMIDDLETON,
S., AND D. LIITTSCHWAGER.
140.
ness: endangered species of North America.
PRINGLE,C. M., AND G. A. BLAKE. 1994. Quantitative
Chronicle Books, San Francisco.
effects of atyid shrimp (Decapoda: Atyidae) on
MILLS,D. 1989. Ecology and management of Atlantic
the depositional environment in a tropical stream:
Salmon. Chapman and Hall, New York.
Use of electricity for experimental exclusion. CaG. W, K. W. CUMMINS,R. C. PETERSON,
C.
MINSHALL,
nadian
Journal of Fisheries and Aquatic Sciences
E. CUSHING,D. A. BRUNS,J. R. SEDELL,
AND R. L.
51:1443-1450.
VANNOTE.1985. Developments in stream ecosysC. M., G. A. BLAKE,A. P. COVICH,K. M. BuzPRINGLE,
tem theory. Canadian Journal of Fisheries and
AND
A. FINLEY.1993. Effects of omnivorous
BY,
Aquatic Sciences 42:1045-1055.
in a montane tropical stream: Sediment
shrimp
F
1995.
California
and
rivers
streams:
the
MOUNT,J.
removal, disturbance of sessile invertebrates and
conflict between fluvial processes and land use.
enhancement of understory algal biomass. OecUniversity of California Press, Berkeley.
ologia 93:1-11.
P.
AND
WILLIAMS.
E.
1990.
MOYLE, B.,
J.
Biodiversity
H. R. 1988. Sources, sinks, and population
PULLIAM,
loss in the temperate zone: decline of the native
American Naturalist 132:652-661.
regulation.
fish fauna of California. Conservation Biology 4:
H. R., AND B. J. DANIELSON. 1991. Sources
PULLIAM,
275-284.
sinks, and habitat selection: a landscape perspecNAIMAN,R. J.,J.J.MAGNUSON,D. M. MCKNIGHT, AND
tive on population dynamics. American NaturalJ. A. STANFORD.1995. The Freshwater Imperaist 137:550-566.
tive: A research agenda. Island Press, WashingAND C. R. GOLDMAN.
RICHEY, J. E., M. A. PERKINS,
ton, DC.
1975. Effects of Kokanee salmon (Oncorhynchus
NAUMANN,M. 1994. A water-use budget for the Canerka) decomposition on the ecology of a subalribbean National Forest of Puerto Rico. Special
stream. Journal of the Fisheries Research
pine
Report, US Department of Agriculture Forest SerBoard of Canada 32:817-820.
vice, Rio Piedras, Puerto Rico.
D. M., R. A. BODALY,AND P. J. USHER.
ROSENBERG,
NEHLSEN, W, J. E. WILLIAMS,AND J. A. LICHATOWICH.
1995. Environmental and social impacts of large
1991. Pacific salmon at the crossroads: stocks at
scale hydroelectric development: who is listenrisk from California, Oregon, Idaho, and WashGlobal Environmental Change 5:127-148.
ing?
ington. Fisheries 16(2):4-21.
SCHLOSSER,I. J. 1995. Dispersal, boundary processes,
R. V. O'NEILL, AND W.
NEWBOLD, J. D., J. W ELWOOD,
and trophic-level interactions in streams adjacent
VAN WINKLE. 1981. Measuring nutrient spiralto beaver ponds. Ecology 76:908-925.
ling in streams. Canadian Journal of Fisheries and
SCHULDT, J. A., AND A. E. HERSHEY.1995. Effect of
Aquatic Sciences 38:860-863.
salmon carcass decomposition on Lake Superior
OSBORNE, L. L., AND M. J. WILEY. 1992. Influence of
tributary streams. Journal of the North American
tributary spatial position on the structure of
Benthological Society 14:259-268.
warmwater fish communities. Canadian Joural
SMITH,L. M., ANDD. M. PATRICK.1991. Erosion, sedof Fisheries and Aquatic Sciences 49:671-681.
imentation, and fluvial systems. Pages 169-181 in
D. M., L. MAO, AND S. T. Ross. 1991. The
PATRICK,
G. A. Kiersch (editor). The heritage of engineering
impact of geomorphic change on the distribution
geology: the first hundred years. Volume 3. Geoof bayou darters in the Bayou Pierre System. Mulogical Society of America, Boulder, Colorado.
seum Technical Report No. 18., Mississippi DeSNODGRASS,J. W. 1996. The influence of beaver ponds
on the temporal and spatial dynamics of southpartment of Wildlife, Fisheries and Parks, Museum of Natural Science, Jackson, Mississippi.
eastern stream fish assemblages. PhD DissertaD. M., S. T. Ross, ANDP. D. HARTFIELD.
1993.
PATRICK,
tion, Institute of Ecology, University of Georgia,
Fluvial geomorphic considerations in the manAthens.
SPENCER, C. N., B. R. MCCLELLAND, AND J. A. STANagement and stewardship of fluvial ecosystems.
FORD. 1991. Shrimp stocking, salmon collapse
Pages 90-99 in Proceedings of a symposium on
and eagle displacement. BioScience 41:14-21.
Riparian ecosystems in the humid US: functions
This content downloaded from 128.192.10.126 on Wed, 3 Jul 2013 11:57:08 AM
All use subject to JSTOR Terms and Conditions
438
C. M. PRINGLE
[Volume 16
US ARMYCORPSOFENGINEERS.
1993. Water need for
Dodge (editor). Proceedings of the International
Puerto Rico: San Juan Metropolitan Region. ReLarge River Symposium. Canadian Special Publication, Fisheries and Aquatic Sciences 106.
port Number 2040-12 to the Puerto Rican Water
and Sewage Authority, San Juan.
WILLIAMS,
J. E., D. B. BOWMAN,AND J. E. BROOKS.
1985. Endangered aquatic ecosystems in North
VAN DEN AVYLE,M. J., ANDJ. W EVANS.1990. TemAmerican deserts with a list of vanishing fishes
perature selection by striped bass in a Gulf of
of the region. Journal of the Arizona-Nevada
Mexico coastal river system. North American
Journal of Fisheries Management 10:58-66.
Academy of Science 20:1-62.
WINSTON,M. R., C. M. TAYLOR,AND J. PIGG. 1991.
VANNOTE, R. L., G. W MINSHALL, K. W. CUMMINS, J.
R. SEDELL,AND C. E. CUSHING.1980. The river
Upstream extirpation of four minnow species due
to damming of a prairie stream. Transactions of
continuum concept. Canadian Journal of Fisheries
the American Fisheries Society 120:98-105.
and Aquatic Sciences 37:130-137.
R. C., M. E. DOUGLAS,AND G. K. MEFFE. WOOTTON,
J. T., AND D. A. BELL.1992. A metapopuVRIJENHOEK,
lations model of the peregrine falcon in Califor1985. Conservation genetics of endangered fish
nia: viability and management strategies. Ecologpopulations in Arizona. Science 228:400-402.
ical Applications 2:307-321.
WARD, J. V., AND J. A. STANFORD. 1989. Riverine ecoReceived:10 May 1996
systems: The influence of man on catchment dynamics and fish ecology. Pages 56-64 in D. P.
Accepted:4 February1997
This content downloaded from 128.192.10.126 on Wed, 3 Jul 2013 11:57:08 AM
All use subject to JSTOR Terms and Conditions