Jonathan M. Bossenbroek

PREDICTION OF LONG‐DISTANCE DISPERSAL USING GRAVITY MODELS: ZEBRA MUSSEL INVASION OF INLAND LAKES

Gravity models are commonly used by geographers to predict migration and interaction between populations and regions. Even though rarely used by ecologists, gravity models allow estimation of long-distance dispersal between discrete points in heterogeneous landscapes. We developed a production-constrained gravity model to forecast zebra mussel (Dreissena polymorpha) dispersal into inland lakes of Illinois, Indiana, Michigan, and Wisconsin (USA) based on the site and location of lakes and the number and location of boats within 364 counties. A deterministic form of this model was used to estimate best-fit parameters for distance coefficient, Great Lakes boat-ramp attractiveness, and colonization cutoff threshold. A stochastic model thus developed from these parameters allows for random changes in colonization likelihood. The results of our model are highly correlated with the actual pattern of colonized lakes in southern Michigan and southeastern Wisconsin at the end of 1997. Areas of central Wisconsin and...

The Potential Distribution of Zebra Mussels in the United States

Abstract The range expansion of zebra mussels (Dreissena polymorpha) in North America has been rapid and costly in both economic and ecological terms. Joint social, political, and scientific ventures such as the 100th Meridian Initiative aim to reduce the spread of zebra mussels by eliminating the unintended transport of the species and preventing its westward expansion. Here we forecast the potential distribution of zebra mussels in the United States by applying a machine-learning algorithm for nonparametric prediction of species distributions (genetic algorithm for rule-set production, or GARP) to data about the current distribution of zebra mussels in the United States and 11 environmental and geological covariates. Our results suggest that much of the American West will be uninhabitable for zebra mussels. Nonetheless, some catchments along the West Coast and in the southeastern United States exhibit considerable risk of invasion and should be monitored carefully. Possible propagule dispersal to these places should be managed proactively.

Boats, Pathways, and Aquatic Biological Invasions: Estimating Dispersal Potential with Gravity Models

Biological invaders can have dramatic effects on the environment and the economy. To most effectively manage these invaders, we should consider entire pathways, because multiple species are dispersed through the same vectors. In this paper, we use production-constrained gravity models to describe movement of recreational boaters between lakes – potentially the most important pathway of overland dispersal for many aquatic organisms. These models are advantageous because they require relatively easily acquired data, hence are relatively easy to build. We compare linear and non-linear gravity models and show that, despite their simplicity, they are able to capture important characteristics of the recreational boater pathway. To assess our model, we compared observed data based on creel surveys and mailed surveys of recreation boaters to the model output. Specifically, we evaluate four metrics of pathway characteristics: boater traffic to individual lakes, distances traveled to reach these lakes, Great Lakes usage and movement from the Great Lakes to inland waters. These factors will influence the propagule pressure (hence the probability of establishment of invasive populations) and the rate of spread across a landscape. The Great Lakes are of particular importance because they are a major entry point of non-indigenous species from other continents, hence will act as the origin for further spread across states. The non-linear model had the best fit between model output and empirical observations with r2 =0.80, r2 =0.35, r2 =0.57, and r2 =0.36 for the four metrics, respectively. For the distances traveled to individual lakes, r2 improved from 0.35 to 0.76 after removal of an outlier. Our results suggest that we were able to capture distances traveled to most but not all lakes. Thus, we demonstrate that production-constrained gravity models will be generally useful for modeling invasion pathways between non-contiguous locations.

Secondary spread of zebra mussels (Dreissena polymorpha) in coupled lake-stream systems 1

ABSTRACT We postulated that dispersal through streams is an important factor in the spread of nonindigenous aquatic species to uninvaded lakes. We tested this hypothesis with zebra mussels (Dreissena polymorpha), whose planktonic larvae are particularly prone to transport through streams. To examine this potential mechanism of spread, we (1) assessed populations of zebra mussels in 2000 and 2003 in coupled lake-stream systems of the St. Joseph River basin (Indiana and Michigan, USA) and (2) examined the interconnectedness of lake-stream systems by evaluating all invaded inland lakes and reservoirs in the United States. We compared observed patterns in zebra mussel populations in 2000 and 2003 to patterns predicted by two proposed models of spread: the static source–sink model and the progressive downstream-march model. Adult zebra mussel densities in lake outflows declined with distance downstream of invaded lakes. Maximum downstream occurrences of adults were variable over the years surveyed, but did not increase through time, suggesting that the source–sink model best fit zebra mussel distributions in these lake-stream couplets. For the conterminous US, we examined the connectedness of inland lakes in close proximity to invaded lakes to determine if stream connections were related to invasions. We also measured the distances between invaded lakes and downstream lakes that were potential recipients of colonists to examine the importance of stream distance in relation to zebra mussel invasions. Lakes connected to invaded lakes were more likely to be invaded than non-connected lakes, and the probability of becoming invaded increased with the proximity between lakes. Our results suggest that a better understanding of the role that streams play as pathways for new biological invasions is crucial for directing management and prevention efforts.

Effects of turbidity and prey density on the foraging success of age 0 year yellow perch Perca flavescens.

Laboratory experiments were conducted to determine how larval and juvenile yellow perch Perca flavescens respond to changes in prey density when exposed to different levels and types of turbidity (phytoplanktonic or sedimentary). Across prey densities, consumption by P. flavescens tended to be less in phytoplanktonic turbidity compared with sedimentary turbidity. For larvae, this effect was dependent on turbidity level (consumption differed between turbidity types only at high turbidity), while for juveniles the difference with turbidity type was equal across turbidity levels. These results suggest that phytoplankton blooms are detrimental to the ability of late season age 0 year P. flavescens to forage and support the need to control factors leading to excessive phytoplankton growth in lakes.

The Influence of Environment, Sex, and Innate Timing Mechanisms on Body Temperature Patterns of Free‐Ranging Black‐Tailed Prairie Dogs (Cynomys ludovicianus)

Mechanisms that influence body temperature patterns in black‐tailed prairie dogs are not well understood. Previous research on both free‐ranging and laboratory populations of black‐tailed prairie dogs (Cynomys ludovicianus) has suggested that reductions in ambient temperature and food and water deprivation are the primary factors that stimulate torpor in this species. In other species, however, torpor has been shown to be influenced by a multitude of factors, including innate circadian and circannual timing mechanisms, energy status, and reproductive behaviors. Our objective was to clarify the influence of weather, sex, and intrinsic timing mechanisms on the body temperature patterns of free‐ranging black‐tailed prairie dogs. We monitored body temperatures of eight adult (>1 yr) prairie dogs from November 1999 to June 2000. Prairie dogs showed distinct daily and seasonal body temperature patterns, which reflected changes in ambient temperatures that occurred during these periods. These patterns of daily and seasonal heterothermy suggest that body temperature patterns of black‐tailed prairie dogs may be driven by an innate timing mechanism. All prairie dogs entered torpor intermittently throughout winter and spring. Torpor bouts appeared to be influenced by precipitation and reductions in ambient temperature. Our results also suggest that reproductive behaviors and circadian timing may influence torpor in this species.

Profiling ecosystem vulnerability to invasion by zebra mussels with support vector machines

Decades since the initial establishment of zebra mussels (Dreissena polymorpha) in North America, understanding and controlling the invasion of aquatic ecosystems continues to be a problem in continent-wide conservation and landscape management. While the high economic and conservation burden of this species makes accurate predictions of future invasions a research priority, forecasting is confounded by limited data, tenuous model assumptions, and the stochasticity of the invasion process. Using a new method for niche identification, we profiled invasion vulnerability for 1,017 lakes in the Great Lakes region of the Unites States. We used a nonparametric geoadditive regression model to test for effects of two water quality variables on the present distribution of zebra mussels. We then used the support vector data description (SVDD), a support vector machine for one-class classification, to estimate the boundary of the ecological niche. By disentangling niche estimation from distributional assumptions, computational niche models could be used to test an array of fundamental concepts in ecology and evolution, while species invasions forecasting is representative of the wide range of potential applications for niche identification in conservation and management.

A sensitive environmental DNA (eDNA) assay leads to new insights on Ruffe (Gymnocephalus cernua) spread in North America

Detection of invasive species before or soon after they establish in novel environments is critical to prevent widespread ecological and economic impacts. Environmental DNA (eDNA) surveillance and monitoring is an approach to improve early detection efforts. Here we describe a large-scale conservation application of a quantitative polymerase chain reaction assay with a case study for surveillance of a federally listed nuisance species (Ruffe, Gymnocephalus cernua) in the Laurentian Great Lakes. Using current Ruffe distribution data and predictions of future Ruffe spread derived from a recently developed model of ballast-mediated dispersal in US waters of the Great Lakes, we designed an eDNA surveillance study to target Ruffe at the putative leading edge of the invasion. We report a much more advanced invasion front for Ruffe than has been indicated by conventional surveillance methods and we quantify rates of false negative detections (i.e. failure to detect DNA when it is present in a sample). Our results highlight the important role of eDNA surveillance as a sensitive tool to improve early detection efforts for aquatic invasive species and draw attention to the need for an improved understanding of detection errors. Based on axes that reflect the weight of eDNA evidence of species presence and the likelihood of secondary spread, we suggest a two-dimensional conceptual model that management agencies might find useful in considering responses to eDNA detections.

Distribution of Native Mussel (Unionidae) Assemblages in Coastal Areas of Lake Erie, Lake St. Clair, and Connecting Channels, Twenty-Five Years After a Dreissenid Invasion

Abstract Over the past 25 years, unionid mussels in the Laurentian Great Lakes of North America have been adversely impacted by invasive dreissenid mussels, which directly (e.g., by attachment to unionid shells) and indirectly (e.g., by competing for food) cause mortality. Despite the invasion, unionids have survived in several areas in the presence of dreissenid mussels. We investigated current spatial patterns in these native mussel refuges based on surveys for unionid mussels across 48 sampling locations (141 sites) in 2011 and 2012, and documented species abundance and diversity in coastal areas of lakes St. Clair and Erie. The highest-quality assemblages of native mussels (densities, richness, and diversity) appear to be concentrated in the St. Clair delta, where abundance continues to decline, as well as in in Thompson Bay of Presque Isle in Lake Erie and in just a few coastal wetlands and drowned river-mouths in the western basin of Lake Erie. The discovery of several new refuge areas suggests that unionids have a broader distribution within the region than previously thought.

A Spatial Modeling Approach to Predicting the Secondary Spread of Invasive Species Due to Ballast Water Discharge

Ballast water in ships is an important contributor to the secondary spread of invasive species in the Laurentian Great Lakes. Here, we use a model previously created to determine the role ballast water management has played in the secondary spread of viral hemorrhagic septicemia virus (VHSV) to identify the future spread of one current and two potential invasive species in the Great Lakes, the Eurasian Ruffe (Gymnocephalus cernuus), killer shrimp (Dikerogammarus villosus), and golden mussel (Limnoperna fortunei), respectively. Model predictions for Eurasian Ruffe have been used to direct surveillance efforts within the Great Lakes and DNA evidence of ruffe presence was recently reported from one of three high risk port localities identified by our model. Predictions made for killer shrimp and golden mussel suggest that these two species have the potential to become rapidly widespread if introduced to the Great Lakes, reinforcing the need for proactive ballast water management. The model used here is flexible enough to be applied to any species capable of being spread by ballast water in marine or freshwater ecosystems.