Kevin L. Pangle

LARGE NONLETHAL EFFECTS OF AN INVASIVE INVERTEBRATE PREDATOR ON ZOOPLANKTON POPULATION GROWTH RATE

We conducted a study to determine the contribution of lethal and nonlethal effects to a predators net effect on a preys population growth rate in a natural setting. We focused on the effects of an invasive invertebrate predator, Bythotrephes longimanus, on zooplankton prey populations in Lakes Michigan and Erie. Field data taken at multiple dates and locations in both systems indicated that the prey species Daphnia mendotae, Daphnia retrocurva, and Bosmina longirostris inhabited deeper portions of the water column as Bythotrephes biomass increased, possibly as an avoidance response to predation. This induced migration reduces predation risk but also can reduce birth rate due to exposure to cooler temperatures. We estimated the nonlethal (i.e., resulting from reduced birth rate) and lethal (i.e., consumptive) effects of Bythotrephes on D. mendotae and Bosmina longirostris. These estimates used diel field survey data of the vertical gradient of zooplankton prey density, Bythotrephes density, light intensity, and temperature with growth and predation rate models derived from laboratory studies. Results indicate that nonlethal effects played a substantial role in the net effect of Bythotrephes on several prey population growth rates in the field, with nonlethal effects on the same order of magnitude as or greater (up to 10-fold) than lethal effects. Our results further indicate that invasive species can have strong nonlethal, behaviorally based effects, despite short evolutionary coexistence with prey species.

River-plume use during the pelagic larval stage benefits recruitment of a lentic fish

Similar to coastal marine systems, Lake Erie exhibits open-water river plumes that differ physicochemically and biologically from surrounding waters. To explore their importance to yellow perch (Perca flavescens) recruitment in western Lake Erie, we tested two related hypotheses: (i) contributions of larvae to the juvenile stage (when recruitment is set) would be greater from nutrient-rich Maumee River plume (MRP) waters than from less-productive non-MRP waters; and (ii) warmer temperatures and higher zooplankton (prey) production in the MRP (versus non-MRP waters) would underlie this expected recruitment difference through “bottom-up” effects on larval growth. Peak larval yellow perch density was 10-fold and 5-fold less in the MRP than in non-MRP waters during 2006 and 2007, respectively. However, otolith microchemical analyses demonstrated that disproportionately more juvenile recruits emanated from the MRP than from non-MRP waters during both years. Although temperature and zooplankton production were ...

Context‐dependent planktivory: interacting effects of turbidity and predation risk on adaptive foraging

By shaping species interactions, adaptive phenotypic plasticity can profoundly influence ecosystems. Predicting such outcomes has proven difficult, however, owing in part to the dependence of plasticity on the environmental context. Of particular relevance are environmental factors that affect sensory performance in organisms in ways that alter the tradeoffs associated with adaptive phenotypic responses. We explored the influence of turbidity, which simultaneously and differentially affects the sensory performance of consumers at multiple trophic levels, on the indirect effect of a top predator (piscivorous fish) on a basal prey resource (zooplankton) that is mediated through changes in the plastic foraging behavior of an intermediate consumer (zooplanktivorous fish). We first generated theoretical predictions of the adaptive foraging response of a zooplanktivore across wide gradients of turbidity and predation risk by a piscivore. Our model predicted that predation risk can change the negative relationship between intermediate consumer foraging and turbidity into a humped-shaped (unimodal) one in which foraging is low in both clear and highly turbid conditions due to foraging-related risk and visual constraints, respectively. Consequently, the positive trait-mediated indirect effect (TMIE) of the top predator on the basal resource is predicted to peak at low turbidity and decline thereafter until it reaches an asymptote of zero at intermediate turbidity levels (when foraging equals that which is predicted when the top predator is absent). We used field observations and a laboratory experiment to test our model predictions. In support, we found humped-shaped relationships between planktivory and turbidity for several zooplanktivorous fishes from diverse freshwater ecosystems with predation risk. Further, our experiment demonstrated that predation risk reduced zooplanktivory by yellow perch (Perca flavescens) at a low turbidity, but had no effect on consumption at an intermediate turbidity. Together, our theoretical and empirical findings show how the environmental context can govern the strength of TMIEs by influencing consumer sensory performance and how these effects can become realized in nature over wide environmental gradients. Additionally, our hump-shaped foraging curve represents an important departure from the conventional view of turbiditys effect on planktivorous fishes, thus potentially requiring a reconceptualization of turbiditys impact on aquatic food-web interactions.

Scaling-up anti-predator phenotypic responses of prey: impacts over multiple generations in a complex aquatic community.

Non-consumptive effects (NCEs) of predators owing to induced changes in prey traits are predicted to influence the structure of ecological communities. However, evidence of the importance of NCEs is limited primarily to simple systems (e.g. two to four species) over relatively short periods (e.g. less than one generation). We examined the NCEs of a fish predator, arising from phenotypic plasticity in zooplankton prey traits, over multiple generations of a diverse zooplankton community. The presence of fish, caged to remove consumptive effects, strongly influenced zooplankton community structure, through both direct and indirect NCE pathways, altering the abundance of many taxa by magnitudes as large as 3 to 10-fold. Presence of fish affected different species of cladocerans and copepods both positively and negatively. A particularly striking result was the reversal of dominance in copepod taxa: presence of fish reduced the ratio of calanoids to cyclopoids from 6.3 to 0.43. Further, the NCE of fish had a strong negative trophic cascade to zooplankton resources (phytoplankton). To our knowledge, this is the first experiment to show that NCEs can influence the abundance of multiple prey species over time spans of multiple prey generations. Our findings demonstrate that adaptive phenotypic plasticity of individuals can scale-up to affect the structure of ecological communities.

The invasive predator Bythotrephes induces changes in the vertical distribution of native copepods in Lake Michigan

Invasive predators can have large negative effects on native prey populations. The susceptibility of native prey to invasive predators may depend on their ability to respond behaviorally to the presence of these non-native predators. In a field survey conducted in Lake Michigan over several years, we found that high densities of the invasive predatory cladoceran Bythotrephes were correlated with lower vertical distributions of some species and age classes of native copepods; moving from inhabiting primarily the epiliminion at low Bythotrephes density to primarily the hypolimnion at high Bythotrephes density. Five groups showed this pattern; diaptomid copepodites, adult cyclopoids, Diacyclops thomasi, and the adult diaptomids Leptodiaptomus ashlandi and L. minutus. In contrast, Bythotrephes density was not correlated with the vertical distribution of copepod nauplii and adult L. sicilis. Laboratory experiments suggest that the changes in the vertical distribution in the field at high Bythothrephes are due to an inducible, plastic response to predation threat from Bythotrephes signaled by water-borne cues. Species that were lower in the field at high Bythotrephes densities responded behaviorally to water-borne cues from Bythotrephes by moving to lower levels of experimental water columns. These species included D. thomasi and L. minutus, with L. ashlandi displaying a non-significant trend in the same direction. In contrast, L. sicilis, which was not correlated with Bythotrephes density in the field, was unaffected by the water-borne cues. Differences in vertical distribution shifts among these native copepod species and life-history stages are likely due to species-specific differences in spatial overlap with Bythotrephes and their relative ability to migrate large distances or employ alternative avoidance strategies. The varied responses exhibited among the copepod groups likely alter their interactions with each other, their resources and other predators, thus revealing the complex effects Bythotrephes can have on invaded communities.

Finely tuned response of native prey to an invasive predator in a freshwater system

Lack of shared evolutionary history reduces the expectation that native prey will detect and respond to invasive predators. Four mechanisms may explain the adaptive response that is nevertheless seen in various systems: prey may perceive the invasive predator through cue similarity with preexisting predators, cues of conspecifics eaten by the invasive predator, a learned response based on experience with the invasive predator (e.g., cue association), and cues from the invasive predator that are specific to it. We performed laboratory experiments in which zooplankton (Daphnia mendotae) responded adaptively to the zooplanktivore Bythotrephes longimanus (migrating downward), showed no response to taxonomically similar predatory cladocerans, and responded adaptively to more taxonomically distant native fish (migrating downward) and native shrimp (migrating upward). Conspecific cues associated with Bythotrephes predation actually reduced the response of D. mendotae to Bythotrephes. Combined with previous experiments that rule out learning, our experiments rule out the first three mechanisms above, demonstrating that D. mendotae respond to cues specific to and produced directly by Bythotrephes. This finely tuned response may be retained from an ancestral species that coevolved with Bythotrephes in its native range, or may have rapidly evolved due to strong selection by the invasive predator.

Temperature gradients, not food resource gradients, affect growth rate of migrating Daphnia mendotae in Lake Michigan

ABSTRACT zooplankton production plays a critical role in the Great Lakes ecosystem, and vertical migration, which is exhibited by many zooplankton species, could affect production. We examined the effects of water temperature and food resource gradients on the growth rate of zooplankton undergoing vertical migration in Lake Michigan. In three laboratory experiments, juvenile Daphnia mendotae, native herbivorous cladocerans, were incubated for 5 days at water temperatures associated with the epilimnion and deep chlorophyll maxima (DCM) of Lake Michigan and were fed food resources collected directly from these regions. Growth rate strongly depended on water temperature, as Daphnia incubated at the epilimnetic temperature (21 °C) grew 42% faster than those at the DCM temperature (8 °C). Growth rate of Daphnia that alternated between the two temperatures every 12 h (0.108 day-1) was similar to the arithmetic average growth rate of the two water temperature treatment extremes (0.110 day-1), suggesting fluctuating temperatures alone do not substantially influence Daphnia growth. In contrast, food resources derived from different depths did not affect growth rate, nor was there a significant interaction between food resource origin and water temperature effects. Our results indicate that vertical migration will reduce growth rate, and hence zooplankton production, through reduced temperature, not from changes in resources. Consideration of the effects of vertical migration, especially given the known variability in this behavior, may substantially improve zooplankton production estimates in the Great Lakes.

Comparison of 13C and 15N discrimination factors and turnover rates between congeneric crayfish Orconectes rusticus and O. virilis (Decapoda, Cambaridae)

Ecological applications of stable isotope analysis are dependent on knowing consumer-diet discrimination factors (Δ) and consumer metabolic turnover rates (m). We used an 80-day laboratory experiment to test for differences in the δ13C, δ15N and m of two species of crayfish (Orconectes rusticus and O. virilis) fed one of two diets (algae wafers and bloodworms). Over the course of the experiment, the δ13C and δ15N signatures of the crayfish approached equilibrium with those of their diets. We fit our data to a growth-based model and found δ13C, δ15N, and m to be largely indistinguishable between species, except in the case of δ15N and m of crayfish on the algae diet. We thus pooled parameters to calculate Δ13C (algae diet: 1.57‰ [95% confidence interval: 0.86–2.35]; bloodworm diet: 0.8‰ [0.14–1.55]) and Δ15N (bloodworm diet: 1.2‰ [0.32–2.11]), and used species-specific data to calculate Δ15N for the algae diet (O. rusticus: 2.54‰ [2.06–3.08]; O. virilis: 3.35‰ [2.53–4.51]). Our results provide values of stable isotope Δ and m for applications to crayfish, and offer a rare comparison of these values between two closely related species and to commonly used literature values.

Behavioral response of Lake Michigan Daphnia mendotae to Mysis relicta

We performed laboratory experiments to determine if Mysis relicta induce changes in the behavior of Daphnia mendotae collected from Lake Michigan. Laboratory results indicate that Daphnia perceived Mysis kairomones and responded by changing their vertical position in cylinders. Experiments using different resource levels, and two procedures to examine the potential effects of the chemical cues from Mysis or from particulate matter or bacteria associated with capture and defecation of prey, suggest that Daphnia detect Mysis via a chemical cue. This is the first laboratory study that we are aware of that indicates that a zooplankton species from the Great Lakes responds behaviorally to an invertebrate predator. Our findings support the hypothesis that changes in vertical distribution of zooplankton associated with changes in invertebrate predator density, observed in previous Great Lakes studies, is due to behavioral responses to reduce predation risk. It is important to understand and quantify such responses, because predator-induced changes in prey behavior represent trait-mediated interactions that can potentially strongly affect prey growth rates, and indirectly affect resources, competitors, and predators of the prey.

Population Structure of Alligator Gar in a Gulf Coast River: Insights from Otolith Microchemistry and Genetic Analyses

AbstractGrowing interest in the Alligator Gar Atractosteus spatula among anglers and fishery managers has inspired efforts to better manage populations. Successful management requires identifying population structure and understanding the distribution of stocks and associated differences in life history. This is particularly important in river systems along the coast of the Gulf of Mexico, where transitions from freshwater rivers to saltwater bays provide the potential for life history diversification. We used otolith microchemistry and genetics to assess population structure of Alligator Gars in the Guadalupe River–San Antonio Bay system, Texas. Lifetime Sr:Ca revealed three, distinct life histories that differed in prevalence across the system. River-resident fish (i.e., fish exclusive to freshwater) were present throughout the river but were most common in the uppermost river reach (74% of upper river fish). Transient fish that used both river and bay habitats were also found throughout the river but w...