Project Summary
Intellectual merit. Human activities have moved thousands of species out of their native ranges, allowing
them to establish populations in new parts of the world. Such alien species have large effects on native
biodiversity and biogeochemical functioning, cause enormous economic damage, and are one of the most
important and least well controlled of human impacts on the world’s ecosystems.
Although the ability of alien species to alter ecosystems and cause economic damage has now been well
demonstrated, the long-term effects of species invasions are poorly understood. Several common
ecological and evolutionary mechanisms may cause the long-term effects of an invader to be very
different from its short-term effects. Nevertheless, long-term studies of the effects of any alien species are
rare, and ecologists are not yet able to predict how an invader’s effects will change through time. It will
be difficult to manage alien species wisely if we do not understand both their short- and long-term effects.
A group of scientists at the Cary Institute has been studying the effects of the zebra mussel (Dreissena
polymorpha), an important invader of the Hudson River ecosystem, for the past 17 years. During the first
~10 years of the invasion, the zebra mussel reduced populations of phytoplankton and small zooplankton
by ~80%, increased summer water clarity by ~45%, increased concentrations of soluble nutrients while
depleting dissolved oxygen concentrations, increased production of littoral plants and macroinvertebrates,
eliminated half of the biomass of the large zooplankton and macroinvertebrates used as food by fish,
devastated populations of native bivalves, and harmed open-water fishes while favoring littoral zone
fishes. In short, this single alien species completely transformed the physical, chemical, and biological
properties of the Hudson River ecosystem.
Now the Cary group is beginning to see evidence that the zebra mussel population and its effects are
changing over the long term. Survival rates of zebra mussels have fallen by a factor of 100. Remarkably,
this drop in survivorship did not reduce the number of zebra mussels in the river, but it has led to
substantially smaller body sizes and filtration rates in the zebra mussel population. At the same time, the
Cary group has measured substantial recovery in populations of small zooplankton, deepwater
macroinvertebrates, and native bivalves, some of which have now nearly reached pre-invasion levels.
The Cary researchers propose to continue their core measurements of the zebra mussel population and its
effects on water chemistry, water clarity, and populations of phytoplankton, zooplankton, bacteria, and
native pearly mussels. Their long-term program will be modified slightly to better track shifts in the size
composition of phytoplankton, populations of cyanobacteria, and ephemeral thermal stratification, which
may interact with zebra mussel grazing to allow blooms of these nuisance algae to develop.
Adding 5-10 years to this study will allow the Cary group to document the remarkable, decadal-scale
changes that are now occurring in the Hudson, substantially increase the power of statistical models to
describe events in the Hudson, and allow researchers to quantify interactions between zebra mussel
grazing and key climatic variables (freshwater flow and temperature).This study will contribute not only
to a better understanding of the zebra mussel (one of the world’s most important invaders) and aquatic
ecosystems, but also provide one of very few detailed studies of the long-term effects of any alien species.
Broader impacts. The results of this research will be used by the agencies that manage the Hudson, and
should help management of invasive species in general. To reach beyond the scientific community, the
Cary researchers propose to disseminate their findings by (1) posting their data on open websites and
responding to requests for data; (2) continuing a highly successful program (the Changing Hudson
Project) that provides lesson materials and training to high school teachers and students and has already
reached >3000 students; (3) working with partners to provide our data and findings to urban middle
school students through the American Museum of Natural History’s “Urban Advantage” program; and (4)
continuing a very active program of outreach through lectures, seminars, training workshops, and
newspaper articles that reach K-12 and college students, teachers, managers, stakeholder groups, and the
general public.
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Results from prior NSF support
We were supported for the past 10 yr by 2 LTREB grants (DEB 0075265: “Developing a long-term
perspective on the response of an aquatic ecosystem to an invasive bivalve,” $300,000, 2000-2005; DEB
0454001: “Long-term response of an ecosystem to an invasive species”, $320,000, 2005-30 June 2010).
The goal of these projects is “to accurately measure the ecological effects of an important alien species,
the zebra mussel, through long-term study of the Hudson River ecosystem.”
We showed that zebra mussels thoroughly transformed the Hudson River ecosystem (Fig. 1). Our major
findings in 2000-2010 were: (1) Zebra mussels and other suspension-feeders can severely depress
phytoplankton and prevent eutrophication in aquatic ecosystems (Caraco et al. 2006); (2) The
composition of the Hudson’s phytoplankton varies greatly from year to year, which appears to be related
more to temperature than zebra mussel grazing (Fernald et al. 2007; Fig. 7); (3) These losses of
phytoplankton and other edible particles caused large changes that ramified throughout the Hudson and
other aquatic ecosystems (Strayer 2009); (4) Zebra mussel populations are capable of a wide variety of
short-term dynamics, including the persistent cycling that we observed in the Hudson (Strayer & Malcom
2006); (5) The Hudson River ecosystem is jointly controlled by hydrology and zebra mussel grazing,
which interact with one another in complex ways (Strayer et al. 2008); (6) As a result of various
ecological and evolutionary mechanisms, the long-term effects of an alien species may be very different
from its short-term effects (Strayer et al. 2006, 2011, Strayer & Malcom 2007a, Pace et al. 2010; see also
Figs. 2-5 below).
We worked hard to disseminate our findings to diverse audiences. LTREB funding in 2000-2010 resulted
in 51 peer-reviewed journal articles and book chapters, 27 presentations at scientific meetings, 44 invited
seminars at colleges and universities, 28 talks to public audiences, 14 talks to K-12 classes, 4 talks to
college classes, and 17 presentations at technical workshops; 17 articles for popular magazines and
newspapers; and a 30-minute radio program. We taught 2 college classes and wrote a book on Hudson
River ecology (Strayer 2011), all of which rely heavily on the LTREB findings. The LTREB contributed
to the training of 1 post-doc, 4 graduate students, 5 undergraduate students, and 9 others. We maintain a
web site on our Hudson research (www.caryinstitute.org/IES_hudson_river.html), and have archived
samples in the collections of the American Museum of Natural History. The LTREB results provide a
major underpinning for “The Changing Hudson Project” (www.caryinstitute.org/chp.html), a web-based
high school curriculum whose development was supported by funding from the NY State Dept of
Environmental Conservation (NYSDEC). A new partnership with the American Museum of Natural
History (funded by an NSF DR K-12 grant) disseminates our data and findings to urban middle-school
students through AMNH’s Urban Advantage program, which reaches >30% of New York City’s schools.
We are producing videos and other teaching materials, and meeting students and their families face to
face. This partnership greatly extends our ability to reach under-represented minorities.
In addition to these findings that resulted directly from LTREB funding, LTREB results provide a strong
framework that supports many studies funded by other sources. In 2000-2010, we used fisheries records
from the NYSDEC and electric utilities to quantify the effects of the zebra mussel invasion on the
Hudson’s fishes (Strayer et al. 2004, Daniels et al. 2005); assessed the ecological functions of wetlands
and vegetated shallow-water habitats (Findlay et al. 2006, Strayer & Malcom 2007, Arrigoni et al. 2008,
Hunsinger et al. 2010); measured the uptake of dissolved organic matter by zebra mussels (Baines et al.
2005, 2007); experimentally investigated the intensification through time of predation on alien species
(Carlsson & Strayer 2009, Carlsson et al. 2009, 2011); and investigated organic carbon age and
processing in the Hudson (Raymond et al. 2004, Maranger et al. 2005, del Giorgio et al. 2006, del Giorgio
& Pace 2008, Caraco et al. 2010). Although not funded by LTREB dollars, these studies would not have
been possible without the essential data and insights provided by the LTREB project.
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Why study the Hudson for ten more years?
As a result of work funded by LTREB and other sources, the effects of the zebra mussel invasion on the
Hudson River are understood in some detail (Fig. 1). Our study is among the most thorough studies of the
ecological effects of any alien species, and often is featured in textbooks (e.g., Kalff 2002, Dodds 2002,
Closs et al. 2003, Allan & Castillo 2007, Primack 2008, Davis 2009). Indeed, one might conclude from
Fig. 1 that the Hudson River-zebra mussel system is so well understood that there is no need for further
study.
Fig. 1. Conventional summary of the effects of the zebra mussel invasion on the Hudson River
ecosystem, showing a diminution of the pelagic food web and a flourishing of the littoral food web.
From Strayer (2009), after Caraco et al. (1997, 2000, 2006), Findlay et al. (1998), Pace et al. (1998),
Strayer & Smith (2001), and Strayer et al. (2004).
On the contrary, we believe that our growing long-term data set has positioned us to answer key questions
about zebra mussels and invasion ecology, and that the next few years are likely to be especially
productive, for two reasons. Most significantly, we have begun to see evidence that the size, functional
attributes, and ecological effects of the zebra mussel population are changing in important ways over a
decadal time-scale (Figs. 2-5). Survival rates of zebra mussels have fallen by a factor of 100, the sizestructure of the zebra mussel population has shifted dramatically, and parts of the ecosystem have begun
to recover towards or even reach pre-invasion conditions. Tracking the dynamics of the Hudson River
ecosystem over the next decade will allow us to measure how the effects of an important invader change
through time, which is one of the largest unanswered questions in invasion ecology (Strayer et al. 2006,
Hawkes 2007, Davis 2009).
In addition, extending the length of our data set will improve our ability to detect and precisely quantify
the effects of the zebra mussels. Although we have what is probably the longest and most comprehensive
data set on a zebra mussel population and its impacts, we still are seriously limited by inadequate
statistical power. For example, we know that zebra mussel grazing interacts in complex ways with
freshwater flow and temperature (Fernald et al. 2007, Strayer et al. 2008), 2 variables that are changing
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with anthropogenic climate change, but our existing data sets are adequate to explore these interactions
only in broad outline. Ten more years of focused data collection will substantially strengthen our
statistical models and sharpen our insights.
Specifically, we propose to concentrate on the following objectives over the next 10 yr: (1) to measure
how the effects of the zebra mussel on the Hudson River ecosystem change over the long term; (2) to
quantify the functional relationships between zebra mussel grazing rates and ecosystem variables; and (3)
to investigate interactions between zebra mussel grazing and the key climatically driven variables of
freshwater flow and temperature.
Background
Long-term invasion dynamics
Biological invasions are now widely recognized as one of the major factors driving the structure and
function of ecosystems (e.g., Mack et al. 2000, Lodge et al. 2006, Lockwood et al. 2007, Crowl et al.
2008, Davis 2009). Alien species affect nearly all parts of the globe and all types of ecosystems, and can
affect populations of native species (leading to local extirpations), biogeochemical cycling, physical
habitat structure, and ecosystem services and economic values. The effects of even a single alien species
can be as large and far-reaching as any human impact on an ecosystem.
Very few studies of the ecological effects of invaders put their findings into a temporal context, however.
Most such studies are of short duration (<3 yr), some done immediately after the invader appears and
others decades or even centuries later, and a surprising 40% of studies did not even mention how long
after the invasion they were done (Strayer et al. 2006). Consequently, ecologists have not often been able
to describe how the impacts of an invader change over the course of time.
Nevertheless, as several authors have now pointed out (e.g., Strayer et al. 2006, Hawkes 2007, Tillberg et
al. 2007, Carlsson et al. 2009), there is every reason to think that the impacts of an invader should change
over time, and that such changes could be large. Several mechanisms can lead to long-term changes in
invader effects. Because invaders can change “the basic rules of existence” (Vitousek 1990) for all
species in the invaded ecosystem, they can drive evolution in the invaded community to use the invader as
a resource or resist its effects (Schaepfer et al. 2005, Strauss et al. 2006, Vellend et al. 2007, Carlsson et
al. 2009). Likewise, the invader may evolve to better fit the new environmental conditions and biotic
communities in which it finds itself (Lee 2002, Koskinen et al. 2002, Lavergne & Molofsky 2007,
Vellend et al. 2007, Prentis et al. 2008, Davis 2009). The functional attributes of both the invader and
members of the invaded community may change through plasticity (Tillberg et al. 2007, Carlsson &
Strayer 2009, Carlsson et al. 2009, Rennie et al. 2009), leading to changes in the impacts of the invader.
Species composition within invaded communities can shift over the long term towards species that are
resistant to the effects of the invader (Sharp & Whittaker 2003, Vanderploeg et al. 2001, 2009, Kroll et al.
2008, Amundsen et al. 2009), or towards species that can use the invader as a resource (Petrie & Knapton
1999, Kelly & Dick 2005, King et al. 2006, Sylvester et al. 2007). The long-term accumulation or
depletion of materials by the invader may lead to long-term biogeochemical or physical changes in the
invaded ecosystem (e.g., Ehrenfeld 2003, Rejmanek et al. 2005, Marchante et al. 2008, Strayer 2009).
Finally, interactions with other temporally variable driving factors (such as hydrology or precipitation)
may lead the impacts of invaders to vary over the long term (Strayer et al. 2006). All of these mechanisms
probably are common in nature, operate over a wide range of time-scales, and could lead to large changes
in the effects of the invader. Although some hypotheses suggest that the effects of the invader should
moderate over the long term as it accumulates enemies (e.g., Hawkes 2007), others mechanisms described
above should cause the effects of the invader to intensify. Thus, at this point it is not clear how much the
effects of an invader will change through time, how much time this will take, or even whether the effects
are likely to increase or decrease. Ours is among the few studies that are comprehensive and long-term
enough to document how an ecosystem changes through time after an invasion.
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The Hudson River ecosystem
The study area is the freshwater, tidal part of the Hudson River, extending from Troy at RKM 248 (i.e.,
river kilometer 248, measured from The Battery in Manhattan) to Newburgh at RKM 100. Sea salt
typically is present only downriver from RKM 100, where zebra mussels and other freshwater animals are
gradually replaced by a brackish-water fauna (Pace & Lonsdale 2006, Strayer 2006). The freshwater tidal
reach of the Hudson is 900 m wide and 8.3 m deep, on average. The water is turbid (Secchi disk
transparency = 0.5-1.5 m), moderately hard (calcium ~27 mg/L), and nutrient-rich (Caraco et al. 1997,
2006). Summer water temperatures usually reach 25-28 oC. Strong tidal currents that reverse direction
every 6 hr generally keep the water column well mixed. The organic carbon budget is dominated by
allochthonous inputs, but phytoplankton and macrophyte production are substantial and ecologically
important (Cole & Caraco 2006). Our intensive studies of the Hudson River ecosystem began in 1986, 6
yr before the outbreak of zebra mussels in the Hudson.
The zebra mussel
The zebra mussel (Dreissena polymorpha) is a small, suspension-feeding bivalve native to fresh and
slightly brackish waters in the Ponto-Caspian region. It spread westward across Europe beginning in the
early 19th century (Kinzelbach 1992), and probably was introduced into North America in the early 1980s
in the ballast water of an ocean-going ship (Carlton 2008). Over the past 25 yr, it has spread widely across
North America (USGS 2010), and is now a dominant species in many lakes and rivers in both Europe and
North America. Because it forms large populations (Strayer 1991, Mellina & Rasmussen 1994), its
suspension-feeding often reduces plankton populations, with consequent effects on water clarity, water
chemistry, littoral food webs, and fish populations (see summaries by MacIsaac 1996, Karatayev et al.
1997, Strayer et al. 1999, Strayer 2009, Higgins & Vander Zanden 2010). Its arrival led to widespread,
catastrophic losses of native bivalves (Ricciardi et al. 1995, Strayer 1999, Strayer & Malcom 2007a), with
some authors predicting global extinctions of >60 species of endemic North American bivalves (Ricciardi
et al. 1998).
Long-term changes in the Hudson River
Zebra mussels first appeared in the Hudson in 1991, and by the end of 1992 constituted more than half of
all heterotrophic biomass (including fish) in the ecosystem (Strayer et al. 1996). The population
undergoes strong cycling, probably because dense populations of adults suppress juvenile recruitment
(Strayer & Malcom 2006). There have been large changes in the Hudson’s zebra mussel population since
the early years of the invasion (Fig. 2). Most significantly, mortality rates have increased enormously over
the past 19 yr (Fig. 2A). Animals from the 1992 year-class (the first large year-class in the river) had a
survival rate of 54%/yr, while animals from the most recent large cohort (2006 year-class) had survival
rates of just 0.6%/yr. Models show that these high mortality rates should decrease the period of
population cycling from 3-4 yr to 1-2 yr (Strayer & Malcom 2006), although we do not yet have a long
enough record to verify that this is occurring in the field.
Although we do not yet understand all the details, predators are at least partly responsible for this 100fold decline in zebra mussel survival rates. Carlsson et al. (2011) showed experimentally that predation by
blue crabs now removes a large part of the zebra mussel population in late summer. Furthermore, fish
taken from the Hudson ate far more zebra mussels than conspecifics taken from nearby waters without
zebra mussels, suggesting that local predators may be adapting to increase per capita consumption rates
on zebra mussels (Fig. 3). Other possible contributors to lower survival include increased disease (Molloy
et al. 1997, Grizzle et al. 2009) or poor physiological condition resulting from overgrazing of
phytoplankton (Vanderploeg et al. 2009, Nalepa et al. 2010).
Whatever their causes, these increased mortality rates have important ecological consequences. The
clearance rate of the Hudson’s zebra mussel population has been dropping (Fig. 2B), and is now only
~1/3 of what it was in the early years of the invasion (although it is still substantial, ~25% of the volume
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Fig. 2. Long-term changes in the Hudson River zebra mussel population. A. Steep decline in survival
rates over time (r2=0.85, p=0.009) (only 6 cohorts were abundant enough for us the estimate survival
rates in the field); B. Long-term decline in clearance rates of the zebra mussel population during the
growing season (June and August) (r2=0.38, p=0.007); C. Long-term shift in the size-structure of the
population towards small animals; each panel shows the abundance of animals of different shell
lengths. From Pace et al. (2010) and Strayer et al. (2011).
of the estuary/day). Perhaps equally important, the size structure of the zebra mussel population has
shifted markedly, so that large mussels are essentially gone from the Hudson (Fig. 2C). This shift could
be important because mussels of different sizes eat different kinds of particles (MacIsaac et al. 1995). In
particular, small mussels can’t eat large particles such as zooplankton. It is a testament to the resilience of
the zebra mussel population that the 100-fold changes in survivorship rates shown in Fig. 2A have had
such modest and subtle effects (Figs. 2B,C). Nevertheless, these changes are now large enough that they
may be changing the ecology of the Hudson.
Several lines of evidence show that the changes in the zebra mussel population may have allowed parts of
the Hudson ecosystem to recover towards pre-invasion conditions (Figs. 4,5). After a long period of low
abundance, planktonic rotifers and nauplii (i.e., small zooplankton) rebounded sharply in 2005, and are
nearly at pre-invasion levels (Pace et al. 2010, Figs. 4A-B). Strikingly, there was no corresponding
recovery of phytoplankton biomass (Fig. 4C), consistent with the idea that the near-disappearance of large
zebra mussels might have allowed the recovery of only the larger plankton. Likewise, following 7 yr of
steep declines leading to near-extirpation, populations of all native bivalves began to recover in 2000
(Fig. 5; Strayer & Malcom 2007), and some have now nearly reached pre-invasion levels (Fig. 5B).
Populations of deepwater benthic animals (i.e., those from unvegetated sites) showed a similar pattern of
steep declines followed by partial recovery (Fig. 5C; Strayer et al. 2011). In contrast, the zoobenthos of
the littoral zone, which probably has been subsidized by increased production of periphyton and
submersed aquatic vegetation resulting from increased water clarity (Caraco et al. 2000, Strayer & Smith
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Fig. 3. Mean consumption
rates (+1SE) of zebra mussels
by (a) pumpkinseed, (b)
redbreast sunfish and (c) rock
bass as a function of prior
exposure to zebra mussels.
“Naive” fish come from sites
where zebra mussels have not
yet appeared, “intermediate”
fish come from sites where
zebra mussels appeared <10
years ago and “experienced”
fish come from sites where
zebra mussels appeared >10
years ago. Significance levels
from Kruskal-Wallis or onetailed Wilcoxon tests are given
on each panel. Note the
difference in scales on the Yaxes. ND=no data. Carlsson &
Strayer (2009).
Fig. 4. Long-term dynamics of (A)
rotifer numbers, (B) nauplius numbers,
and (C) phytoplankton biomass in the
Hudson River, showing recent recovery
of small zooplankton but not
phytoplankton. Pace et al. (2010).
2001), showed no clear pattern of decline and recovery (Fig. 5D). The community composition of the
deepwater zoobenthos (but not littoral zoobenthos) also shifted after zebra mussels arrived, then returned
towards its pre-invasion composition in 2005-2006 (Strayer et al. 2011). All of this evidence shows that
the post-invasion Hudson ecosystem has been dynamic rather than static, and may be undergoing
directional changes (i.e., recovery).
Proposed research
The central long-term goals of our LTREB research will continue to be the quantitative description of the
zebra mussel population and its effects on the Hudson River ecosystem; and how the population and its
effects change through time. Our previous research provides an exceptional foundation for examining the
dynamic nature of an invasion through time. Over the next 5-10 yr, we will focus specifically on 3 areas:
(1) documenting whether and how the decadal-scale changes that we are beginning to see in the zebra
mussel population and its effects continue to develop; (2) quantifying the functional relationships between
the size and characteristics of the zebra mussel population and the Hudson ecosystem; (3) investigating
interactions between zebra mussel grazing and key climatic variables.
Documenting decadal-scale changes in the invader and its effects
Hypotheses
H1. Mortality rates of zebra mussels will remain high, leading to a dominance of small-bodied
mussels and low to moderate population clearance rates.
This hypothesis is based on an extrapolation of observed trends (Fig. 2), as well as our experiments that
suggest rising mortality from predators (Carlsson & Strayer 2009, Carlsson et al. 2011). We see no reason
to expect these trends to reverse in the coming decade.
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Fig. 5. Long-term dynamics of zoobenthic populations in the Hudson River: (A) the large pearly
mussel Elliptio complanata; (B) the tiny pea clam Pisidium spp.; (C) deepwater macrobenthos; and
(D) littoral macrobenthos. Note the logarithmic y-axes in (A) and (B). Densities in (C) and (D) are
expressed as residuals from log10-transformed means at each sampling station to filter out large
spatial variation in the data. All of these variables except for littoral zoobenthos show an apparent
change in dynamics about 2000. Updated from Strayer & Smith (2001), Strayer & Malcom (2007a),
and Strayer et al. (2011).
H2. The zebra mussel population will continue to cycle on a short period (1-2 yr), leading to large,
short-term fluctuations in population size and clearance rates (Fig. 2B).
Simulation models (Strayer & Malcom 2006) show that increasing mortality should first shorten the
period of population cycles, then cause the population to crash completely. Because mortality from
predators is focused in late summer, after zebra mussels have reproduced (Carlsson et al. 2011), we do not
believe that mortality will be high enough to cause the zebra mussel population to collapse.
H3. Various parts of the Hudson River ecosystem will recover towards pre-invasion levels. Such
recovery will be asynchronous, and will be greatest during periods of low clearance rates by the
zebra mussel population and for items too large to be eaten by small zebra mussels.
The recovery of various ecosystem components is likely to be idiosyncratic because (1) the direct effects
of a declining zebra mussel population are likely to be nonlinear (Fig. 6) and different between different
parts of the ecosystem (Figs. 4A vs. 4C), depending on their characteristics (e.g.,
response time, which varies from days for phytoplankton and bacteria to years for unionids and vascular
plants) and on whether they respond more to a reduction in bulk grazing rates or to a shift in the sizestructure of the zebra mussel population; (2) indirect effects are also likely to be nonlinear and
differentially propagated through the ecosystem; and (3) the degree to which various recovery
mechanisms (e.g., evolution, species shifts) operate, and the time-scales on which they operate, will vary
across different parts of the ecosystem. The complexity of the potential responses, along with the paucity
of previous studies on the long-term effects of invaders, means that it is not possible to confidently
predict the Hudson’s response a priori. Instead, we need to measure its actual responses.
Core measurements. - Our ongoing long-term program of measurements (Table 1) documents temporal
and spatial variation in many key parts of the Hudson River ecosystem, from physical and chemical
variables to plankton populations and benthic animals, including the zebra mussel population itself. We
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propose to modify this ongoing program only slightly over the next few years to address our first 3
hypotheses.
Table 1. Core measurements on the Hudson River made with LTREB funding. Details on methods for
sampling and analysis were given by Findlay et al. (1998), Pace et al. (1998, 2010), Findlay (2005),
Caraco et al. (2006), and Strayer & Malcom (2006, 2007).
Variable
Time period
Spatial extent
Zebra mussel (and quagga mussel) population
(density, biomass, size structure)
1991- (biannual)
Entire river
Phytoplankton (biomass)
1986- (biweekly)
One site
Phytoplankton (biomass)
1986- (bimonthly)
Entire river
Zooplankton (density, species composition)
1986 – (biweekly)
One site
Zooplankton (density, species composition)
1986- (bimonthly)
Entire river
Water quality (transparency, nutrients)
1986- (weekly)
One site
Water quality (transparency, nutrients)
1986- (bimonthly)
Entire river
Seston, particulate and dissolved organic C
1987- (biweekly)
One site
Seston, particulate and dissolved organic C
1987- (bimonthly)
Entire river
Bacterial abundance and production
1987- (biweekly)
One site
Bacterial abundance
1987- (bimonthly)
Entire river
Native unionid mussels (density, species composition,
body condition)
1991- (annual)
Entire river
Additions to field sampling. - Our current sampling program gives us only limited information on
phytoplankton composition. Because we suspect that changes in the size-structure of the zebra mussel
population (Fig. 2) may affect its ability to control particles of different sizes, we propose to size-fraction
phytoplankton samples before chlorophyll analysis. Samples will simply be filtered through a 20-µm
mesh Nitex screen before analysis. We also propose to augment our measurements of water temperature
and cyanobacterial densities as described below.
Although LTREB funding is insufficient to allow us to sort the samples of benthic invertebrates other
than bivalves, we propose to use the LTREB funding to take and archive samples of benthic invertebrates
using established protocols (Strayer & Smith 2001, Strayer et al. 2011) every 2-3 yr. Such samples are
relatively simple to collect but very time-consuming to process. We hope to be able to attract other
funding to support the processing of these samples.
Statistical analyses. - Methods to estimate the density, size-structure and mortality rates of the zebra
mussel population were described by Strayer & Malcom (2006). We use a stratified random design to
sample both hard and soft substrates throughout the river, identify species (zebras vs. quaggas) measure
shell length and body mass in large subsamples of animals collected from the field, and use finite mixture
analysis in R (Du 2002) to quantitatively separate cohorts.
We will use 2 methods to test for recovery in ecosystem components. For pelagic variables (which are
measured every 2 wk), we will use time-series analysis (Wei 2005, Box et al. 2008) of data collected
since 1993 (i.e., post-zebra mussel), to test whether there has been either (1) a significant positive
intervention, or (2) an overall positive slope over time. In addition to the intervention term, we will
include time and freshwater flow as independent variables. We have only annual samples of unionid
mussels and zoobenthos, so data will be too few to support time-series models. Instead, we will use
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piecewise regression with a single breakpoint (Marsh & Cormier 2001, Seber & Wild 2003) to look for
evidence of recovery as either (1) a significant 2-regression model, with the later slope more positive than
the earlier slope, or (2) an overall positive slope in a 1-regression model.
Quantifying the functional relationships between the invader and the ecosystem
H4: The effects of zebra mussels on various parts of the Hudson ecosystem will depend on the
number and body size of zebra mussels, and many of these relationships will be nonlinear.
Most often, ecologists use a binary approach to assess the effects of an invasion; i.e., they just compare
conditions before the invasion to conditions after the invasion. This certainly is a reasonable first
approach to the problem of describing the effects of an invader. However, if the population size or
functional characteristics (e.g., body size) of the invader vary over time or across sites, then its effects
should likewise vary. It is rare for ecologists to have sufficient data to describe the functional
relationships between the abundance of an invader and its effects in the field. However, it will be
necessary to move beyond a simple binary approach to invasions if we are to understand and manage the
effects of alien species. For instance, information on the shape and parameters of the function linking the
abundance of an alien species to its effects could be used to set the threshold at which undesirable effects
occur (and thus, the point at which management might be warranted) or to set targets for restoration (i.e.,
the amount by which the population of the alien must be reduced to achieve desired goals).
Fig. 6. Response of 2 parts of the Hudson River ecosystem to variation in zebra mussel grazing rates.
A. phytoplankton biomass responds to total grazing rates; B. rotifer numbers respond to grazing rates
of large mussels (shell length >20mm) (based on Caraco et al. 2006, Pace et al. 2010).
Our early assessments of the effects of the zebra mussel on the Hudson River ecosystem likewise treated
the presence-absence of zebra mussels as a binary variable (e.g., Fig. 1). This was justified because we
had too few data to quantify the relationship between zebra mussel grazing and ecosystem characteristics,
and because clearance rates in early years of the invasion were so high that we never observed the
response of the system at low grazing rates. However, our post-invasion data set has grown to cover 19
yr, and zebra mussel grazing rates have at times fallen below <1% of their peak rates (Fig. 2B), so we are
beginning to be able to quantify the relationship between grazing rates and ecosystem responses. So far,
we have modeled only phytoplankton biomass and microzooplankton numbers as a function of grazing
rates (Fig. 6). Both relationships are nonlinear, but phytoplankton biomass depends on the total grazing
rate, whereas microzooplankton numbers depend on the grazing rate of just the largest mussels.
Generally, we expect that relationships between zebra mussel grazing and ecosystem components will be
nonlinear, and will not be congruent across different parts of the ecosystem (i.e., we would not expect
dissolved oxygen or zoobenthic populations to follow the same curve as phytoplankton biomass). We
expect that the size-structure of the zebra mussel population will affect the response of some parts of the
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ecosystem (i.e., parts of the ecosystem such as microzooplankton that can be grazed by large mussels but
not small mussels, or which depend on such variably grazed components).
With 5-10 years more of data, we will have enough data points (n~30 annual means and n~600 biweekly
samples for most parts of the ecosystem) covering the full range of variation of grazing rates to begin to
quantify the relationships between zebra mussel grazing and ecosystem responses.
Statistical analyses. – We will model the relationships between zebra mussel filtration rates and various
parts of the Hudson River ecosystem (Table 1). Several variations of these models will be run: (1) linear
vs. exponential fits (the latter has been described for phytoplankton and would be expected from simple
models – Caraco et al. 2006); (2) total filtration rate of the zebra mussel population vs. size-fractionated
filtration rates. For the latter, we will estimate the filtration rate of 3 sizes of zebra mussels (shell length =
0-10, 10-20, and 20+ mm) in the river using our field data on densities and sizes of zebra mussels in the
river and Kryger & Riisgard’s (1988) regressions of filtration rate vs. body size in zebra mussels (which
agree well with measured filtration rates of Hudson River animals – Roditi et al. 1996, 1997). We will use
biweekly data in time-series models for pelagic variables, and annual means in regression models for
benthic variables, and will include freshwater flow as a covariate.
These analyses will help us decide whether any recovery that we document (see above) is likely to be
partly or primarily a result of long-term declines in filtration rates or body size of zebra mussels (Fig. 2),
or may better be attributed to other mechanisms.
Investigating interactions between zebra mussel grazing and climatic variables
Although zebra mussel grazing is a dominant factor that controls the character of the Hudson River
ecosystem, it is not the only important factor. In particular, short-term and interannual variation in
freshwater flow (discharge) and temperature also appear to be important in determining ecosystem
structure and function, and appear to interact with zebra mussel grazing. These variables are of special
interest because both are likely to change as a result of human-induced climate change in the coming
decades (e.g., Scavia et al. 2002, UCS 2006). It is clear both that short- and long-term variation in climate
can affect the structure and function of estuaries and other aquatic ecosystems in complex ways (e.g.,
Scavia et al. 2002, Cloern et al. 2007, 2010, Kimmel et al. 2009, Winder et al. 2009), and that data often
have been insufficient to do the necessary analyses (e.g., Cloern et al. 2010). If we are to predict and
understand the effects of 21st century climate change on aquatic ecosystems, we will need to collect the
data to support stronger analyses of the effects of climate variables, and how these variables interact with
other drivers such as species invasions.
Our preliminary analyses show that freshwater flow and temperature may interact in interesting and
complex ways with zebra mussel grazing (Fernald et al. 2007, Strayer et al. 2008), but the precision of
these analyses was badly limited by the amount of available data. Climate change in the Northeast is
predicted to produce lower freshwater flows during the growing season (UCS 2006). The amount of
freshwater flow affects many parts of the Hudson River ecosystem, and interacts with zebra mussel
grazing, sometimes in surprising ways (i.e., both positive and negative interactions; Strayer et al. 2008).
Because this analysis was based on just 18 yr of data for most parts of the ecosystem, we were able to
explore only a small number of models, all of them linear, and our estimates of model parameters were
necessarily imprecise (typically, we could not statistically detect effect sizes smaller than ~2-fold). After
5-10 more years of data collection, we will have 29-34 yr of data on most parts of the ecosystem, which
will allow us to substantially improve the power and insights of these models.
Although interannual variation in water temperature has a small or undetectable effect on some parts of
the ecosystem (Strayer et al. 2004), it may be of key importance in regulating the appearance of nuisance
blooms of cyanobacteria (Fig. 7). Water temperatures in the Hudson have been rising since the 1940s
(Ashizawa & Cole 1994, Kaushal et al. 2010), and are predicted to continue rising (UCS 2006). High
summer water temperatures are strongly associated with cyanobacterial blooms (Fig. 7). Fernald et al.
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13.5
13.0
12.5
12.0
11.5
11.0
Grazing rate
50
% cyanobacteria
Mean annual temperature (oC)
14.0
40
30
20
Blooms
rare
10
10.5
10.0
Blooms likely
0
1950
1960
1970
1980
1990
2000
2010
23
24
25
26
August temperature (oC)
27
Summer temperature
Fig. 7. Possible temperature effects on dominance of cyanobacteria in the Hudson. Left: long-term
increases in Hudson River temperature (Kaushal et al. (2010). Center: relationship between August
water temperatures and dominance of the Hudson’s phytoplankton by cyanobacteria in 1993-2005
(Fernald et al. 2007). Right: Hypothetical relationship between temperature, zebra mussel grazing
rates, and outbreaks of cyanobacteria in the Hudson.
(2007; see also Howarth et al. 2000) hypothesized that high summer water temperatures lead to ephemeral
stratification of the Hudson (which usually is well mixed vertically in its freshwater reaches), allowing
colonial cyanobacteria to escape grazing and grow to a size at which they are unpalatable to zebra
mussels (Bastviken et al. 1998, Vanderploeg et al. 2001, 2009).
H5: The water column of the Hudson will stratify when warm temperatures, neap tides, low
freshwater flow, and low wind speeds coincide.
H6: Nuisance blooms of colonial cyanobacteria will occur either (1) during warm periods in which
the river stratifies; or (2) when zebra mussel grazing rates are very low (Fig. 7).
H7: Nuisance blooms of cyanobacteria will become more frequent in the Hudson as water
temperatures rise and grazing rates of zebra mussels fall.
Additions to field sampling. - To address Hypotheses 5-7, we propose to augment our sampling program
by adding a vertical thermistor chain to make the high-frequency, vertically distributed measurements of
water temperature needed to detect ephemeral stratification. We will use 3 complementary methods to
estimate densities of cyanobacteria. First, we will deploy a YSI 6131 sonde equipped with a phycocyanin
probe at 1m depth. Our experience with this probe in lakes suggests it will register the presence of
cyanobacteria at least when they become abundant. The
continuous record will produce readings every 15 min, making a rich time-series to analyze. During July
and August, we will augment our usual sampling by taking samples for phycobiliproteins and algal
species composition. Large water samples (several liters) for phycobiliproteins will be filtered through
glass fiber filters, which will be frozen. Total phycobiliproteins will be measured by spectrofluorometry
using the method of Kursar & Alberte (1983). These discrete samples will be used to calibrate the
automated sensor and act as a backup in case of sensor failure. Samples for algal species composition
(using the methods described by Fernald et al. 2007) will be taken and archived, and will be analyzed if
the pigment data are unsatisfactory. Sensors will be co-located with the HRECOS instruments (see below)
near our long-term sampling station near Kingston.
Statistical analyses. – Our analysis of the effects of freshwater flow will build on our earlier analyses
(Strayer et al. 2008).We will use multiple regression models based on the normalized, growing-season
means of dependent variables (Table 1). In addition to simple linear models, our larger data set will allow
us to test models with exponential decay functions for grazing and freshwater flow, the form expected
from theoretical models (e.g., Caraco et al. 2006, Lucas et al. 2009; cf. Fig. 6).
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We will model the occurrence of persistent stratification (defined as a temperature difference >0.5C
between the top and bottom of the water column that persists for >24 hr – i.e., long enough to allow
cyanobacteria to grow (Robarts & Zohary 1987, Fogg 1991, Sherman et al. 1998)) using time-series
models with mean water temperature, freshwater flow (from the USGS gage at Green Island), and wind
speed and tidal range data from the real-time distributed network of sampling stations (www.hrecos.org)
as independent variables. We will use linear regression to model abundance of cyanobacteria as a function
of water temperature, zebra mussel grazing, and time (Fernald et al. 2007).
Related research
Our group is conducting several projects that are related to the LTREB work. We collaborate with several
other organizations to support a continuous, real-time network of water quality monitoring sites in the
Hudson (www.hrecos.org). These fixed locations span RKM 50-220 and provide important temporal
context for the bi-weekly or bi-monthly LTREB sampling. Findlay and Strayer recently received funding
from the Hudson River Foundation to conduct a change analysis for submerged aquatic vegetation in the
tidal freshwater Hudson. Documenting areal change in this extensive habitat type is beyond the scope of
LTREB but may be a key link between zebra mussel-influenced changes in water clarity and littoral
primary production.
We are aware that several obvious, important research questions (e.g., the causes of increased mortality of
zebra mussels, the ability of zebra mussels of different sizes to capture different kinds of particles,
comparison of other systems invaded by benthic grazers) are not addressed in this LTREB proposal. Their
omission here simply reflects the very limited budget available under LTREB, and the need to maintain
the core measurements of our LTREB program. We will seek funding from non-LTREB sources to
investigate these questions.
Broader impacts
Data dissemination
Our plans to manage and disseminate our data are described in detail in the supplementary material of this
proposal. Basically, we propose to continue to use several avenues to disseminate our data to a wide range
of users, including other scientists, managers, teachers, students of various ages, and members of the
general public.
Education and outreach
We will use 4 approaches to disseminate our findings beyond the scientific community. First, educators
and scientists at the Cary Institute have developed The Changing Hudson Project, a web-based, high
school curriculum designed to connect students with current research about the Hudson
(www.caryinstitute.org/chp.html). The CHP has been funded primarily by the New York State
Department of Environmental Conservation. We work closely and frequently with the CHP educators (2
of us serve as co-directors of the CHP) to craft the ideas and concepts that will be conveyed to students,
provide data, and ensure that the lesson plans are scientifically accurate. In 2006-2009, the CHP reached
>3000 students at 29 participating schools throughout the Hudson Valley, and trained >200 teachers at
professional development workshops. The CHP web site currently receives >500 unique hits/month. We
will continue to work with the CHP over the coming years to expand, test, and improve the materials that
they provide to students and teachers.
Second, we just began a partnership with the American Museum of Natural History (funded by an NSF
DR K-12 grant) to disseminate our data and findings to urban middle-school students and their families
through AMNH’s Urban Advantage program, which reaches >30% of New York City’s schools. We are
producing videos and written materials, and are meeting students and their families face to face. This
partnership greatly extends our ability to reach under-represented minorities.
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Third, we routinely share our findings with the public through lectures to the public, K-12 classes, staff of
the NYSDEC, and stakeholder groups; participation in technical workshops to train teachers and others;
and newspaper and magazine articles (see “Results from prior NSF support” for a statistical summary of
these efforts), as well as the more traditional seminars, peer-reviewed publications, and presentations at
scientific meetings. We see this individual outreach as an essential part of our efforts, and will continue to
enthusiastically participate in such outreach.
Fourth, we often work with partners who do environmental education to see that our findings reach a
broad audience of stakeholders. One of us serves as a member of the Hudson River Estuary Management
Advisory Committee, and our ideas and findings routinely appear in the goals, recommendations, and
assessments of New York State’s Hudson River Estuary Program (www.dec.ny.gov/lands/4920.html),
such as Stanne et al. (2009). We also work with outreach experts at New York State Sea Grant and
Cornell University (www.css.cornell.edu/iris/rip/hudson/coastlinesarticle.htm,
www.css.cornell.edu/iris/rip/hudson/SAVFactSheet.pdf) to produce outreach materials and programs.
In addition to these efforts, we will continue to train undergraduate and graduate students as part of this
LTREB. The Cary Institute has had a successful REU program since 1988, and has now trained 224 REU
students. This program includes targeted efforts to attract and retain members of under-represented
minorities (28% of students). We also bring in undergraduate and graduate students to Hudson research as
Polgar Fellows (www.hudsonriver.org/polgar.htm) and through other programs. The LTREB will
continue to be a rich source of material for student projects over the next 10 yr.
Management
The primary motivation for our research is to improve basic understanding of the workings of aquatic
ecosystems and how ecosystems respond to species invasions over the long term. Nevertheless, the work
that we propose has obvious utility for managers (indeed, our findings are used routinely managers of the
Hudson). It will continue to provide valuable information about the actual impacts of zebra mussels,
which will help managers decide how much effort to put into programs to prevent the establishment of
new populations, reduce the size of established populations, or mitigate the effects of established
populations. Our models of how impacts vary with the number or size of zebra mussels can be used to set
thresholds at which management might be initiated. Finally, our results should help managers decide
whether the effects of zebra mussels are better treated as permanent, or as transients, against which shortterm measures might be effective.
Significance
The chief contribution of this research will be to document how the ecological effects of a dominant
invader change through time. Ecologists know that alien species are one of the largest human impacts on
the earth’s ecosystems, and that such impacts ought to change over the course of the invasion, but very
few examples actually measure the effects of an invader over the long term. Because both the acute
(short-term) and chronic (long-term) effects of an invader are of interest to managers and scientists, it is
essential that we understand how these impacts change over time. We know that zebra mussels have had
strong, far-reaching effects on the Hudson ecosystem (Fig. 1), and now have strong evidence that these
effects are changing over time (Figs. 2-5). Thus, if we are funded to follow the effects of the zebra mussel
invasion on the Hudson over the next 5-10 yr, we would be almost uniquely well positioned to address
one of the most important questions in invasion ecology.
Second, adding 5-10 more yr to our long-term record will allow us to substantially strengthen our
statistical models and our understanding of this system both by increasing the degrees of freedom and
allowing us to observe the system under a wider range of conditions (especially grazing rates and climatic
variables). As a result, we will be able to much better answer questions about how the condition of the
Hudson ecosystem depends on the size and functional attributes (not just the presence) of the zebra
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mussel population, and its interactions with other driving variables such as freshwater flow and
temperature.
Response to reviews of a previous submission
We submitted versions of this proposal to the Population and Community Ecology program (July 2009)
and the Ecosystems program (Jan 2010). The chief criticisms of the first submission were (1) we did not
plan to investigate the mechanisms behind changes in zebra mussel demography; (2) we did not deal
explicitly with effects of changes in land use and pollution that might be concurrent with zebra mussel
effects; (3) we did not mention plans to train students; (4) we did not show how our results could be
generalized to other systems; (5) we did not connect our work to the many long-term studies of zebra
mussels in Europe; (6) we did not have a plan to engage under-represented groups; (7) we ignored the
likely invasion of the quagga mussel; (8) we did not use power analyses to show that a longer data record
would substantially improve statistical power. Here are our responses.
1) We strongly agree that the mechanisms behind the changes in zebra mussel demography are
interesting, but it is simply impossible to investigate them in detail as part of this proposal, because of the
cap on LTREB budgets ($90K/yr) and the LTREB requirement to maintain core measurements (Table 1).
We have used other sources of funding to investigate the mechanisms behind changes in zebra mussel
demography (Carlsson & Strayer 2009, Carlsson et al. 2011), and will continue to seek non-LTREB
funding to pursue this work. However, the data on zebra mussel populations in the Hudson collected
under LTREB funding (Fig. 2) will be essential to any detailed demographic analysis.
2) Land use and pollution do affect the ecology of the Hudson (e.g., Limburg & Schmidt 1990, Howarth
et al. 1991, Caraco & Cole 1999, Caraco et al. 2010), but land use and pollution loads have changed much
more slowly than zebra mussel populations or the ecosystem variables that we track, and have been
relatively stable over the study period (Swaney et al. 2006). No land-use or pollution variable is a viable
candidate to explain the large, sudden changes in the ecosystem that we observed.
3) We rewrote the proposal to better describe our plans to train students.
4) The Hudson, like every ecosystem, is in some ways unique, so it is fair to ask how results from any
single system can be generalized. Generalizing beyond the Hudson has always been one of our central
goals. We do this by constructing conceptual or quantitative frameworks based on variables that allow
rigorous comparisons across ecosystems, such as water residence time, grazing rates, or time since
invasion, or by building models that allow us to explore the consequences of variation in such key
variables. We have thus effectively extended many of our findings to aquatic ecosystems or ecosystems in
general (e.g., Caraco et al. 1997, 2006, Strayer et al. 1999, 2006, Strayer & Malcom 2006, 2007a).
5) We agree that the European literature provides valuable comparisons to our results, which we have
used in past studies (e.g., Strayer 1991, Strayer & Smith 1993, Strayer & Malcom 2006). Unfortunately,
few long-term data have been published on European zebra mussel populations, contrary to the reviewer’s
assertion, and most of these are compromised by poor sampling methods or large temporal gaps. Thus, it
is not practical to rely heavily on analyses of European data to answer the questions that we pose here.
6) We expanded our plans to engage under-represented groups.
7) Quagga mussels (a relative of the zebra mussel, introduced into North America ~1990, which have
displaced zebra mussels from some sites) first appeared in the Hudson in 2008, but still represent <1% of
the Dreissena population. Our proposed sampling program will track the quagga mussel population as
well as the zebra mussel population. Although there are interesting biological differences between the 2
species, from the viewpoint of ecosystem impacts (filtration rates, food selection, gross impacts on other
parts of the ecosystem) they appear to be similar (e.g., Mills et al. 1996, Ackerman 1999, Baldwin et al.
2002, Stoeckmann 2003, Garton et al. 2005, Nalepa et al. 2009). The expansion of the quagga mussel
population (if it occurs) does not pose a problem for the proposed research.
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8) It is difficult to address this criticism concisely, because we propose to test multiple hypotheses with
many dependent variables, each with its own variance. We agree that in some cases 5-10 yr more of data
will increase statistical power only modestly; it is hardly necessary to collect more data to demonstrate
that the arrival of zebra mussels depressed phytoplankton biomass (Fig. 4C). On the other hand, our
current data sets are too small to run models with very many independent variables, so it has been
difficult or impossible for us to test models with non-linear terms, interactions, or size-structured grazing
(see below). Likewise, the piecewise linear models that we propose to use to test for recovery will require
additional data to adequately estimate slopes and the location of breakpoints. Also, even the limited
models that we have been able to run with existing data typically have been unable to detect effect sizes
less than about 2-fold (Strayer et al. 2008). For these reasons, 5-10 yr more of data will be enormously
helpful in strengthening most of our statistical models.
The second version of this proposal was rated as “Outstanding” by the Ecosystems panel, which wrote
“This is perhaps the best long-term record of the effects of an invasive species on any ecosystem, and the
data set will become even more valuable with continued study. The potential that the ecosystem may be
recovering from an invasive species and that this recovery will be documented is exciting”. However,
they identified 5 weaknesses: (1) our hypotheses were weak, especially concerning climate; we needed to
better pursue (2) comparative studies, (3) spatial analyses, and (4) dynamic models; and (5) we needed
better data management. We agree that points 2-4 represent promising research directions, but think that it
is unrealistic that these could be added to the core measurements that we propose to make within the
constraints of an LTREB budget ($90K/yr). As we have done in the past, we will pursue these
opportunities using other sources of funding (as described in “Results from prior NSF support”). With
respect to points 1 and 5, we substantially reworked and sharpened our hypotheses, and improved our data
management plan.
Going through 2 rounds of review over the past 18 months has certainly improved our proposal, but any
further delay in securing funding for this project will result in gaps in the long-term records. Our current
funding ran out in July 2010 (no-cost-extended to July 2011), and we do not have other sources of
funding to support the core LTREB measurements in 2011.
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