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Evolution of Invasive Species: Characterization and Effects of Adaptive Changes in Bythotrephes Tail Spine
Primary Investigator:
Doran Mason - NOAA/GLERL
Co-Investigators:
Scott Peacor - Michigan State University*
Andrea Jaeger - Michigan State University*
Andrew McAdam - Michigan State University*
Executive Summary of Rationale
The predatory cladoceran
Bythotrephes longimanus (the spiny water flea) has been identified as one of
several recent invasive species of great threat to the Great Lakes (Shuter and Mason 2001;
Vanderploeg et al. 2002; Barbiero and Tuchman 2004). As with other aquatic exotic species,
Bythotrephes has the potential to affect ecosystems through competition with and
predation on native species (Ludsin and Wolfe 2001), by altering nutrient cycles
(Mack et al. 2000), and shifting the direction of energy flow (Mills et al. 2003; Jaeger
2006). Such ecosystem effects of invasive species affect society in numerous ways (Mills
et al. 1994; Hall and Mills 2000; Facon et al. 2005), including damaging commercial and
recreational fisheries (Mills et al. 1994). Bythotrephes may be particularly
disruptive to the food web, causing direct and indirect effects on fish stocks and the
broader food web, because of its central place in the food web between top predators
and secondary producers (Vanderploeg et al. 2002; Figure 1). Most previous studies
investigating the dynamics of food web disruption have focused on changes in the abundance
of invaders. However, changes in interaction strengths can be as or more important to
the overall effect of an invader, yet these effects have only begun to be investigated.
We propose to build on and expand current ecological work by investigating the effects
of rapid evolutionary changes in an exotic species on its trophic interactions. That
is: we will investigate whether evolutionary processes affect the ecology of invasive
species, which in turn would influence their spread and effects. This research is
designed to: 1) specifically, increase our understanding of Bythotrephes
effects on fish and lower trophic levels in the food web; and 2) more generally,
determine how evolution affects food web properties including resilience and
species interaction strengths.
Proposed Work
Current/Ongoing
We propose to quantify contemporary phenotypic and genotypic variation in tail spine length of Great Lakes Bythotrephes using quantitative genetics techniques. We will test whether the size of the spine in Bythotrephes mediates a life history trade-off between the survival benefits of a longer spine and its fecundity costs. We further propose that the relative importance of gape-limited predation dictates the resolution of this trade-off, driving the evolution of spine morphology. We will, therefore, look for evidence of evolutionary changes in this important trait associated with Bythotrephes establishment within novel North American predator communities. The negative effects of spine length on fish consumption are well established, but we will further test the food web consequences of evolutionary changes since the arrival of Bythotrephes in North America by performing predation experiments between naïve and contemporary Bythotrephes and Daphnia mendotae resurrected from deep and shallow sediment layers, respectively.
Scientific Rationale
The complexities of food web disruption by the invasion of Bythotrephes and other invertebrate species in the Great Lakes demand novel and integrative approaches to understanding and managing invasion. As a result, there is a global trend in fisheries and aquatic systems management in which the complex forces affecting ecosystems are examined from an ecosystem perspective (Christensen et al. 1996).
We propose that
current ecosystem approaches to understanding invasion and forecasting future
consequences can be strengthened by recognizing that the abundance and dynamics of
predators and prey are affected by both: 1) species densities; and 2) the magnitude
of species interactions (Figure 2). Although a relatively simple concept, it is
important to recognize that both species density and species interactions can change
through time. It is often implicitly accepted that density effects dominate ecosystem
processes. In contrast, the dynamic nature of species interactions is typically not
considered, although ecologists are becoming increasingly aware of the importance of
changes in species interactions. In particular, species can modify phenotypically
plastic traits over relatively short time scales, including morphological, behavioral,
physiological, and life history traits. At longer time scales, natural selection can
drive genetically based (evolutionary) changes in these same traits. In both cases,
traits that dictate interaction strengths change through time. Most previous studies
of the effects of invasive species have treated invading and native organisms as
static players within a food web (Lambrinos 2004). But focusing exclusively on density
effects ignores dynamics in interaction strengths, which can cause demographic models
of invasion to fail over large spatial and temporal scales (Lee 2002). Unfortunately
little is known about the causes and consequences of changes in interaction strengths
in invaded food webs.
We propose to examine the effect of Bythotrephes on Great Lakes ecosystems, with emphasis on the dynamic nature of interactions between predators and prey. We propose that evolutionary and phenotypically plastic changes in a conspicuous trait of Bythotrephes, its long protective tail spine, have had important implications for species interactions and food web dynamics in Great Lakes ecosystems.
Effects of Bythotrephes Invasion
Bythotrephes
is an efficient predator of both large and small-bodied zooplankton (Schulz and Yurista 1999;
Vanderploeg et al. 2002; Witt and Cáceres 2004), but is also a relatively large
and conspicuous potential prey item for many young fish and adult planktivores
(Pothoven et al. 2003). Bythotrephes has been implicated in shifting the size
structure and abundance of the zooplankton community, even in the presence of
planktivorous fish (Wahlström and Westman 1999). Coincident with invasion, the
abundance of Leptodora kindtii, Daphnia mendotae, D. pulicaria,
and D. retrocurva declined, although D. mendotae later rebounded
(Lehman and Cáceres 1993; Barbiero and Tuchman 2004). Bythotrephes
consumptive demands are quite large; bioenergetic analyses indicate that their energetic
needs approach the daily replacement rate for herbivorous cladocerans in Lake Michigan
(Yurista and Schulz 1995). This heavy grazing suggests severe effects on zooplankton
since invasion (Schulz and Yurista 1999; Barbiero and Tuchman 2004). There is, therefore,
strong evidence that Bythotrephes affects zooplankton assemblages that comprise
the primary prey resource of larval and juvenile fish (e.g., Mills et al. 1992; Lehman
& Cáceres 1993; Dumitru et al. 2001; Vanderploeg et al. 2002).
By consuming large-bodied zooplankton, Bythotrephes is a competitor with young-of-year (YOY) and planktivorous adult fish, and therefore, can have deleterious effects on recruitment and survival. For example, the timing of the yellow perch decline in Lake Michigan closely followed Bythotrephes invasion (Vanderploeg et al. 2002; Dettmers et al. 2003). Bythotrephes can also affect fish by disrupting a fish’s foraging ability (Barnhisel and Kerfoot 2004). Several adult fish depend on Bythotrephes as prey including alewife (Alosa pseudoharengus; Mills et al. 1992), yellow perch (Schneeberger 1991; Baker et al. 1992), and rainbow smelt (Osmerus mordax; Parker et al. 2001) among others (Compton and Kerfoot 2004). Fish consumption of Bythotrephes (and their spines) can lead to fish injury (Compton and Kerfoot 2004) and increase the handling time for small fish. This can reduce growth and increase mortality. Finally, recent precipitous declines in Lake Huron alewife (Johnson et al. 2005), and decreased condition of Pacific salmon (Oncorhynchus spp.), have been hypothesized to result from voracious planktivory by Bythotrephes during late summer (Eshenroder, R.L. pers. comm.).
Trait-Mediated Effects of Invaders
Ecological effects of Bythotrephes depend not just on the number of invading individuals but also on interaction strengths between Bythotrephes and native species (Werner and Peacor 2003; Fig. 2). Changes in interaction strengths cause predator “nonlethal effects” (also called trait-mediated effects). In this case, the predator causes a change in prey phenotype, including behavioral, physiological, life-history, or morphological traits, which in turn affect the interaction strength between predator and prey. For example, Daphnia are known to respond to predators by modifying the timing and depth of vertical migrations, modifying swimming motions and speed, reducing foraging rates, and increasing the size of morphological defenses (reviewed in Tollrian and Harvell 1999). These traits are modified in the presence of predators in order to reduce the predator’s ability to detect, capture or consume the prey (i.e., the interaction strength). K.L. Pangle and S.D. Peacor demonstrated that predator nonlethal effects on Daphnia in Lake Michigan can be much greater (up to 10 fold) than lethal effects (Fig. 3). While perhaps surprising, this remarkable result is supported by theory developed specifically for Lake Michigan. Therefore, the nonlethal effect of a predator can contribute substantially to the net effect of the predator, even overwhelming density effects caused by consumption. Since Bythotrephes is both a zooplankton predator and fish prey (as in Figure 1), it has likely not only induced trait changes in zooplankton but also adjusted its own phenotype to better avoid fish predation.
Evolutionary Change over Ecological Time Scales: Trait Mediated Effects due to Evolution
Individual differences in per capita interaction strength can also change due to species evolution (see Box 1). Evolution and genetics are important to our understanding of the process and effects of invasion because 1) the genetics of key traits can influence a species’ ability to successfully invade, and 2) traits important to interactions with native species, and hence the net ecosystem effect of the invasion, can continue to evolve even after establishment (Lee 2002).
Evolution of Trophic Linkages
Here we defien the evolution of trophic linkages to be genetically based changes in
traits affecting interaction strengths within a food web
Recent examples of rapid contemporary evolution (on time scales of years or decades; e.g., Reznick et al. 1997; Grant and Grant 2002; Réale et al. 2003; McAdam and Boutin 2004) have highlighted the relevance of evolutionary changes to conservation biology and management (reviewed by Stockwell et al. 2003). For example, evolutionary changes in the diapause phenology of a freshwater copepod (Onychodiaptomus sanguineus) in response to fish predation (Hairston and Dillon 1990) were calculated to have occurred at about one quarter the rate of ecological changes in the abundance of fish predators (Hairston et al. 2005). Anthropogenic changes in environmental conditions are thought to be particularly important to rapid contemporary evolutionary change (Palumbi 2001). In particular, many examples of rapid evolutionary change have resulted from the novel selective pressures associated with biological invasions (see Reznick and Ghalambor 2001; Mooney and Cleland 2001). Despite the potential for rapid evolutionary adaptation of invaders to their novel environment (Lambrinos 2004) and native species to the arrival of an exotic species we still know little about the importance of these evolutionary changes to food web dynamics.
Bythotrephes Tail Spine as an Important Trait for Food Web Interactions
The conspicuous antipredatory tail spine of Bythotrephes is an effective deterrent against gape-limited fishes (‹100 mm in length), causing the predator fish to reject or avoid Bythotrephes as prey (Branstrator 2005; Compton and Kerfoot 2004). Several studies have documented avoidance or inability of small fish to consume Bythotrephes, including YOY yellow perch, alewife, rainbow smelt, rainbow trout (Oncorhynchus mykiss), lake whitefish (Coregonus clupeaformis), and lake herring (Coregonus artedi; Barnhisel 1991a; Barnhisel 1991b; Schneeberger 1991; Baker et al. 1992; Barnhisel and Harvey 1995; Compton and Kerfoot 2004). This long spine can comprise over 10% of adult body mass (Sullivan and Lehman 1998, Branstrator 2005) and 80% of body length (Barnhisel and Harvey 1995). Such a heavy investment in post-contact anti-predatory defenses contrasts with some native planktivorous cladocerans, such as L. kindtii, that specialize in pre-contact defenses like transparency (Branstrator 2005). As a result, the length of the spine appears to represent a key trait influencing food web dynamics in the Great Lakes and surrounding inland waters.
Short-term Evolution of Tail Spines since Arrival in the Great Lakes
Longer spines appear to benefit Bythotrephes through increased avoidance by fish predators (Compton and Kerfoot 2004; Barnhisel 1991b), thereby enhancing early survival (Sullivan and Lehman 1998). This benefit of longer spines, however, likely comes at a cost of decreased predatory ability or reduced fecundity due to energetic or structural constraints as seen in other cladocerans (Caramujo and Boavida 2000). As such, spine length in Bythotrephes might represent a life history trade-off between the survival benefits of a longer spine and its fecundity costs.
Changes in spine length in response to changes in the relative importance of these costs and benefits will have important implications for food web dynamics because of the direct effects of spine length on fish consumption. Observed seasonal changes in spine lengths in both the Great Lakes (Bilkovic and Lehman 1997) and Europe (Straile and Hälbich 2000) have been interpreted as resulting from seasonal life history responses to the relative frequency of gape-limited and non-gape-limited fishes. The degree to which these seasonal changes in morphology are due to evolutionary responses to size-selective fish predation is not known. Furthermore, if this seasonal pattern of selection for larger spines late in the growing season is not opposed by fecundity benefits of smaller spines earlier in the season, then we would expect the seasonal evolutionary “ratcheting” of spine length to result in a net evolutionary elongation of Bythotrephes spine since invasion. Observed differences in distal spine (i.e., spine segment between the tip and first barb) lengths among Great Lakes (Sullivan and Lehman 1998) as well as between North America and Europe (Straile and Hälbich 2000) suggest that differences in the relative importance of gape-limited versus non-gape-limited predators might have resulted in local adaptation of spine lengths. This hypothesized evolutionary elongation of the spine will reduce consumption rates by gape-limited fishes.
If there is a trade-off between the survival benefits of a longer spine and reduced ability to capture prey, any adjustment of Bythotrephes spine length to fish predation will have implications for interactions between Bythotrephes and its prey.
Hypothesis
We hypothesize that contemporary variation in tail spine length in Bythotrephes
is the result of survival selection favoring longer spines and fecundity selection favoring
shorter spines. We further suggest that differences in the relative importance of
gape-limited predation of Bythotrephes has resulted in the evolution of spine morphology
since arrival in North America. These hypothesized evolutionary changes have important
direct consequences for fish consumption as well as consequences for interactions with
Bythotrephes prey such as Daphnia.
Governmental/Societal Relevance
Managers in the Great Lakes and surrounding inland waters are increasingly using an ecosystem perspective when creating management strategies. Ecosystem management entails managing systems given our best understanding of the processes necessary to sustain ecosystem composition, structure and function (Christensen et al. 1996). The National Oceanic and Atmospheric Administration (U.S. Department of Commerce National Oceanic and Atmospheric Administration 2004) has committed to ecosystem management, as have other government agencies including the Great Lakes Fishery Commission (Great Lakes Fishery Commission 2001), the U.S. Fish and Wildlife Service (U.S. Fish and Wildlife Service 1994; Beattie 1996), the U.S. Environmental Protection Agency (U.S. Environmental Protection Agency 1999), and the Canadian Wildlife Service (Wildlife Ministers’ Council of Canada 1990).
Our proposed research contributes to this effort in ecosystem management by investigating rapid contemporary evolutionary change – an understudied but valuable approach to elucidating the causes and consequences of ecosystem change – in the shaping of trophic linkages involving Bythotrephes, a species of concern for the integrity of the Great Lakes (Shuter and Mason 2001). Our research integrates established techniques for examining species change, including sediment core analysis and resurrection ecology (e.g., Hairston et al. 1999; Kerfoot et al. 2004; Kerfoot and Weider 2004), within the context of exotic species invasion. Additionally, our research examines Bythotrephes effects in Great Lakes and inland lake systems where comparative work is lacking. In their paper on food web disruptions of invasive invertebrates, Shuter and Mason (2001) argue that: 1) life history characteristics of invasive species can govern how food webs are disrupted; and 2) by comparing ecosystems we can draw generalities about invaders and predict future change. By examining the effects of important traits of Bythotrephes on trophic linkages in multiple ecosystems, we can shed light onto the mechanisms of food web disruption by invasive species, and inform management at the ecosystem level.
Relevance to Ecosystem Forecasting
Relevance to Ecosystem Forecasting overlaps directly with the previous section on Governmental / Societal relevance. The proposal aims to identify and increase our understanding of a factor that affects Great Lakes food webs, and thereby add to our ability to build forecasting models.
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