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Nicholas A. Friedenberg

Senior Scientist
Applied Biomathematics
Setauket, NY


Martinez, J.C., N.A. Friedenberg, and M.A. Caprio. Density dependence and growth rate: evolutionary effects on resistance development to Bt (Bacillus thuringiensis). Journal of Economic Entomology
Accepted paper. Preprint not yet available.

It has long been recognized that pest population dynamics can affect the durability of a pesticide, but dose remains the primary component of insect resistance management (IRM). For transgenic pesticidal traits such as Bt (Bacillus thuringiensis), dose (measured as the mortality of susceptibles caused by a toxin) is a relatively fixed characteristic and often falls below the standard definition of high dose. Hence, it is important to understand how pest population dynamics modify durability and what targets they present for IRM. We used a deterministic model of a generic arthropod pest to examine how the timing and strength of density dependence interact with population growth rate and Bt mortality to affect time to resistance.

As in previous studies, durability typically reached a minimum at intermediate doses. However, high population growth rates could eliminate the benefit of high dose. The timing of density dependence had a more subtle effect. If density dependence operated simultaneously with Bt mortality, durability was insensitive to its strengths. However, if density dependence was driven by post-selection densities, decreasing its strength could increase durability. The strength of density dependence could affect the durability of both single traits and pyramids, but its influence depended on the timing of density dependence and the size of the refuge.

Our findings suggest the utility of a broader definition of high dose, one that incorporates population-dynamic context. That maximum growth rates and the timing and strength of the interactions causing density dependent mortality can all affect durability also highlights the need for ecologically integrated approaches to IRM research.

Friedenberg, N.A., J.J. Hoover, K. Boysen, and K.J. Killgore. Estimating abundance without recaptures of marked pallid sturgeon in the Mississippi River. Conservation Biology DOI: 10.1111/cobi.12972
Accepted paper. Request preprint.

Abundance estimates are essential for estimating the viability of populations and the risks posed by alternative management actions. An effort to estimate abundance via a repeated mark-recapture experiment may fail to recapture marked individuals. We present a framework for obtaining lower bounds on abundance in the absence of recaptures for both panmictic and spatially-structured populations. We applied this nil-recapture method to data from a 12-year survey of pallid sturgeon (Scaphirhynchus albus) in the lower and middle Mississippi River; none of the 241 individuals marked were recaptured in the survey. After accounting for survival and movement, our model-averaged estimate of the total abundance of age 3+ pallid sturgeon in the study area had a 1%, 5%, or 25% chance of being less than 4,600, 7,000, or 15,000, respectively. If we assumed fish were distributed in proportion to survey catch-per-unit-effort, then the furthest downstream reach in the survey hosted at least 4.5-15 fish per river kilometer (rkm), whereas the remainder of the reaches in the lower and middle Mississippi River hosted at least 2.6-8.5 fish rkm-1 for all model variations examined. The lower Mississippi River had an average density of at least 3.0-9.8 age-3+ pallid sturgeon rkm-1. The choice of Bayesian prior was the largest source of uncertainty considered in this study, but did not alter the order of magnitude of lower bounds. Nil-recapture estimates of abundance are highly uncertain and require careful communication but can deliver insights from experiments that might otherwise be considered a failure.

Powell, J.A., M.J. Garlick, B.J. Bentz, N.A. Friedenberg. 2018. Differential dispersal and the Allee effect create power-law behavior: distribution of spot infestations during mountain pine beetle outbreaks. Journal of Animal Ecology 87:73-86.
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  1. Mountain pine beetles (MPB, Dendroctonus ponderosae Hopkins) are aggressive insects attacking Pinus host trees. Pines use defensive resin to overwhelm attackers, creating an Allee effect requiring beetles to attack en masse to successfully reproduce. MPB kill hosts, leaving observable, dying trees with red needles. Landscape patterns of infestation depend on MPB dispersal, which decreases with host density. Away from contiguously impacted patches (low beetle densities), infestations are characterized by apparently random spots (of 1-10 trees).
  2. It remains unclear whether the new spots are spatially random eruptions of a locally endemic population or a mode of MPB spread, with spatial distribution determined by beetle motility and the need to overcome the Allee effect.
  3. To discriminate between the hypothesis of population spread versus independent eruption, a model of spot formation by dispersing beetles facing a local Allee effect is derived. The model gives rise to an inverse power distribution of travel times from existing outbreaks. Using landscape-level host density maps in three study areas, an independently-calibrated model of landscape resistance depending on host density, and aerial detection surveys, we calculated yearly maps of travel time to previous beetle impact. Isolated beetle spots were sorted by travel time and compared with predictions. Random eruption of locally endemic populations was tested using artificially-seeded spots. We also evaluated the relationship between number of new spots and size of the perimeter of previously infested areas.
  4. Spot distributions conformed strongly to predicted power-law behavior. The spatially random eruption hypothesis was found to be highly improbable. Spot numbers grew consistently with perimeter of previously infested area, suggesting that MPB spread long distances from the boundary via spots following an inverse power distribution.
  5. The Allee effect in MPB therefore accelerates, rather than limits, invasion rates, contributing to recent widespread landscape-scale mortality in western North America.

Friedenberg, N. and C. Foley. 2016. Defining protection of endangered species from an integrated multispecies perspective. Technical Report 3002008418. Electric Power Research Institute, Palo Alto, CA.
download pdf from EPRI website

With respect to conservation planning, the United States has for some time been moving toward multispecies approaches. This shift recognizes the fundamental ecological fact that species do not exist in isolation, and it is thus possible to move from reactive to proactive management in order to reduce the need for future listings under the Endangered Species Act (ESA). Conservation aimed at higher ecological scales such as landscapes and ecosystems creates opportunities for coordination of conservation actions and public-private partnerships. This report examines the integrated multispecies perspective on management of endangered species.

Friedenberg, N. and K.T. Shoemaker. 2014. RAMAS IRM version 2.0: Software for risk-based durability assessment. Applied Biomathematics, Setauket, NY
RAMAS website

RAMAS® IRM (Insect Resistance Management) is a software platform for modeling the risk of pest adaptation to Bt crops under a broad range of resistance management strategies. The tool has enough flexibility to address all major insect crop pests through user-defined life histories.

IRM modeling investigates the complex interaction of insect pest population dynamics and population genetics with agricultural technology and farming practices. The total integration of landscape, demography, and evolution places IRM at the cutting edge of landscape genetics and applied evolution.

Our goal is to provide a common platform for IRM modeling that fosters both transparency and innovation in the devlopment and management of transgenic pesticidal crops. A guiding principle in the development of this flexible tool is that it should remove barriers to powerful modeling. That means pushing the limits of what is currently practical in terms of complexity while keeping the software easy to use even for beginning modelers.

Thomas, M.J., M.L. Peterson, N. Friedenberg, J.P. Van Eenennaam, J.R. Johnson, J.J. Hoover, A.P. Klimley. 2013. Stranding of spawning run green sturgeon in the Sacramento River: post-rescue movements and potential population-level effects. North American Journal of Fisheries Management 33:287-297.
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The lower portion of the Sacramento River, California, has been highly engineered to protect low-lying surrounding communities from annual flood events. While engineered floodplains have provided adequate protection for the surrounding communities, there remain unintended consequences to migratory fish that become stranded during high flow events. In April, 2011, we rescued 24 threatened Green Sturgeon (Acipenser medirostris) that were stranded in two flood diversions along the Sacramento River. We tagged these 24 Green Sturgeon with acoustic tags and analyzed their survival and migration success to their spawning grounds. Additionally, we provided a population viability analysis to show the potential impacts of stranding and the benefits of conducting rescues at the population level. We found that 17 of these 24 individuals continued their upstream migration to the spawning grounds.Modeling suggests that recurrent stranding of a similar magnitude without rescue could affect the long-term viability of Green Sturgeon in the Sacramento River. Population viability analyses of rescue predicted a 7% decrease below the population baseline model over 50 years as opposed to 33% without rescue. Despite the mitigated impact to the population with rescue, fish passage improvements should be considered as a long-term goal for preventing population risks at flood control diversions.

Dennehy, J.J., N.A. Friedenberg, R.C. McBride, R.D. Holt, and P.E. Turner. 2010. Experimental evidence that source genetic variation drives pathogen emergence. Proceedings of the Royal Society, Series B 277: 3113-3121.
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A pathogen can readily mutate to infect new host types, but this does not guarantee successful establishment in the new habitat. What factors, then, dictate emergence success? One possibility is that the pathogen population cannot sustain itself on the new host type (i.e. host is a sink), but migration from a source population allows adaptive sustainability and eventual emergence by delivering beneficial mutations sampled from the source’s standing genetic variation. This idea is relevant regardless of whether the sink host is truly novel (host shift) or whether the sink is an existing or related, similar host population thriving under conditions unfavourable to pathogen persistence (range expansion). We predicted that sink adaptation should occur faster under range expansion than during a host shift owing to the effects of source genetic variation on pathogen adaptability in the sink. Under range expansion, source migration should benefit emergence in the sink because selection acting on source and sink populations is likely to be congruent. By contrast, during host shifts, source migration is likely to disrupt emergence in the sink owing to uncorrelated selection or performance tradeoffs across host types. We tested this hypothesis by evolving bacteriophage populations on novel host bacteria under sink conditions, while manipulating emergence via host shift versus range expansion. Controls examined sink adaptation when unevolved founding genotypes served as migrants. As predicted, adaptability was fastest under range expansion, and controls did not adapt. Large, similar and similarly timed increases in fitness were observed in the host-shift populations, despite declines in mean fitness of immigrants through time. These results suggest that source populations are the origin of mutations that drive adaptive emergence at the edge of a pathogen’s ecological or geographical range.

Friedenberg, N.A., S. Sarkar, N. Kouchoukos, R.F. Billings, M.P. Ayres. 2008. Temperature extremes, density dependence, and southern pine beetle (Coleoptera: Curculionidae) population dynamics in east Texas. Environmental Entomlogy 37: 650-659
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Previous studies of the southern pine beetle, Dendroctonus frontalis Zimm., established that its population in east Texas responds to a delayed density-dependent process, whereas no clear role of climate has been determined.We tested two biological hypotheses for the influence of extreme temperatures on annual southern pine beetle population growth in the context of four alternative hypotheses for density-dependent population regulation. The significance of climate variables and their interaction with population regulation depended on the model of density dependence. The best model included both direct and delayed density dependence of a cubic rather than linear form. Population growth declined with the number of days exceeding 32 C, temperatures previously reported to reduce brood survival. Growth was highest in years with average minimum winter temperatures. Severely cold winters may reduce survival, whereas warm winters may reduce the efficiency of spring infestation formation. Whereas most previous studies have incorporated climate as an additive effect on growth, we found that the form of delayed density dependence changed with the number of days over 32 C. The interaction between temperature and regulation, a potentially common phenomenon in ecology, may explain why southern pine beetle outbreaks do not occur at perfectly regular intervals. Factors other than climate, such as forest management and direct suppression, may have contributed significantly to the timing, severity, and eventual cessation of outbreaks since the mid-1950s.

Friedenberg, N.A., B.M. Whited, D.H. Slone, S.J. Martinson, M.P. Ayres. 2007. Differential impacts of the southern pine beetle, Dendroctonus frontalis, on Pinus palustris and Pinus taeda. Canadian Journal of Forest Research 37: 1427-1437
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Patterns of host use by herbivore pests can have serious consequences for natural and managed ecosystems, but are often poorly understood. Here, we provide the first quantification of large differential impacts of the southern pine beetle, Dendroctonus frontalis Zimmermann, on loblolly pine, Pinus taeda, and longleaf pine, P. palustris, and evaluate putative mechanisms for the disparity. Spatially extensive survey data from recent epidemics indicate that, per km2, stands of loblolly vs. longleaf pine in four forests (380-1273 km2) sustained 3-18 times more local infestations and 3-116 times more tree mortality. Differences were not attributable to size or age structure of pine stands. Using pheromone-baited traps, we found no differences in the abundance of dispersing D. frontalis or its predator, Thanasimus dubius Fabricius, between loblolly and longleaf stands. Trapping triggered numerous attacks on trees, but the pine species did not differ in the probability of attack initiation, nor in the surface area of bark attacked by growing aggregations. We found no evidence for post-aggregation mechanisms of discrimination or differential success on the two hosts, suggesting that early colonizers discriminate between host species before a pheromone plume is present.

Friedenberg, N.A., J.A. Powell, M.P. Ayres. 2007. Synchrony's double edge: transient dynamics and the Allee effect in stage structured populations. Ecology Letters 10: 564-573
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In populations subject to positive density dependence, individuals can increase their fitness by synchronizing the timing of key life history events. However, phenological synchrony represents a perturbation from a population’s stable stage structure and the ensuing transient dynamics create troughs of low abundance that can promote extinction. Using an ecophysiological model of a mass-attacking pest insect, we show that the effect of synchrony on local population persistence depends on population size and adult lifespan. Results are consistent with a strong empirical pattern of increased extinction risk with decreasing initial population size. Mortality factors such as predation on adults can also affect transient dynamics. Throughout the species range, the seasonal niche for persistence increases with the asynchrony of oviposition. Exposure to the Allee effect after establishment may be most likely at northern range limits, where cold winters tend to synchronize spring colonization, suggesting a role for transient dynamics in the determination of species distributions.

Dennehy, J.J., N.A. Friedenberg, Y. Yang, P.E. Turner. 2007. Virus population extinction via ecological traps. Ecology Letters 10: 230-240
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Populations are at risk of extinction when unsuitable or when sink habitat exceeds a threshold frequency in the environment. Sinks that present cues associated with highquality habitats, termed ecological traps, have especially detrimental effects on net population growth at metapopulation scales. Ecological traps for viruses arise naturally, or can be engineered, via the expression of viral-binding sites on cells that preclude viral reproduction. We present a model for virus population growth in a heterogeneous host community, parameterized with data from populations of the RNA bacteriophage U6 presented with mixtures of suitable host bacteria and either neutral or trap cells. We demonstrate that viruses can sustain high rates of population growth in the presence of neutral non-hosts as long as some host cells are present, whereas trap cells dramatically reduce viral fitness. In addition, we demonstrate that the efficacy of traps for viral elimination is frequency dependent in spatially structured environments such that population viability is a nonlinear function of habitat loss in dispersal-limited virus populations. We conclude that the ecological concepts applied to species conservation in altered landscapes can also contribute to the development of trap cell therapies for infectious human viruses.

Dennehy, J.J., N.A. Friedenberg, Y. Yang, P.E. Turner. 2006. Bacteriophage migration via nematode vectors: host-parasite-consumer interactions in laboratory microcosms. Applied and Environmental Microbiology 72: 1974-1979
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Pathogens vectored by nematodes pose serious agricultural, economic, and health threats; however, little is known of the ecological and evolutionary aspects of pathogen transmission by nematodes. Here we describe a novel model system with two trophic levels, bacteriophages and nematodes, each of which competes for bacteria. We demonstrate for the first time that nematodes are capable of transmitting phages between spatially distinct patches of bacteria. This model system has considerable advantages, including the ease of maintenance and manipulation at the laboratory bench, the ability to observe many generations in short periods, and the capacity to freeze evolved strains for later comparison to their ancestors. More generally, experimental studies of complex multispecies interactions, host-pathogen coevolution, disease dynamics, and the evolution of virulence may benefit from this model system because current models (e.g., chickens, mosquitoes, and malaria parasites) are costly to maintain, are difficult to manipulate, and require considerable space. Our initial explorations centered on independently assessing the impacts of nematode, bacterium, and phage population densities on virus migration between host patches. Our results indicated that virus transmission increases with worm density and host bacterial abundance; however, transmission decreases with initial phage abundance, perhaps because viruses eliminate available hosts before migration can occur. We discuss the microbial growth dynamics that underlie these results, suggest mechanistic explanations for nematode transmission of phages, and propose intriguing possibilities for future research.

Dennehy, J.J., N.A. Friedenberg, R.D. Holt, P.E. Turner. 2006. Viral ecology and the maintenance of novel host use. American Naturalist 167: 429-439
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Viruses can occasionally emerge by infecting new host species. However, the early phases of emergence can hinge upon ecological sustainability of the virus population, which is a product of both within-host population growth and between-host transmission. Insufficient growth or transmission can force virus extinction before the latter phases of emergence, where genetic adaptations that improve host use may occur. We examined the early phase of emergence by studying the population dynamics of RNA phages in replicated laboratory environments containing native and novel host bacteria. To predict the breadth of transmission rates allowing viral persistence on each species, we developed a simple model based on in vitro data for phage growth rate over a range of initial population densities on both hosts. Validation of these predictions using serial passage experiments revealed a range of transmission rates for which the native host was a source and the novel host was a sink. In this critical range of transmission rates, periodic exposure to the native host was sufficient for the maintenance of the viral population on the novel host. We argue that this effect should facilitate adaptation by the virus to utilize the novel host—often crucial in subsequent phases of emergence.

Friedenberg, N.A. 2003. Determinism in a transient assemblage: the roles of dispersal and local competition. American Naturalist 162: 586-596
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Both dispersal and local competitive ability may determine the outcome of competition among species that cannot coexist locally. I develop a spatially implicit model of two-species competition at a small spatial scale. The model predicts the relative fitness of two competitors based on local reproductive rates and regional dispersal rates in the context of the number, size, and extinction probability of habitat patches in the landscape. I test the predictions of this model experimentally using two genotypes of the bacteriophagous soil nematode Caenorhabditis elegans in patchy microcosms. One genotype has higher fecundity while the other is a better disperser. With such a fecundity-dispersal trade-off between competitors, the model predicts that relative fitness will be affected most by local population size when patches do not go extinct and by the number of patches when there is a high probability of patch extinction. The microcosm experiments support the model predictions. Both approaches suggest that competitive dominance in a patchily distributed transient assemblage will depend upon the architecture and predictability of the environment. These mechanisms, operating at a small scale with high spatial admixture, may be embedded in a larger metacommunity process.

Friedenberg, N.A. 2003. Experimental evolution of dispersal in spatiotemporally variable microcosms. Ecology Letters 6: 953-959
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The world is an uncertain place. Individuals' fates vary from place to place and from time to time. Natural selection in unpredictable environments should favour individuals that hedge their bets by dispersing offspring. I confirm this basic prediction using Caenorhabditis elegans in experimental microcosms. My results agree with evolutionary models and correlations found previously between habitat stability and individual dispersal propensity in nature. However, I also find that environmental variation that triggers conditional dispersal behaviour may not impose selection on baseline dispersal rates. These findings imply that an increased rate of disturbance in natural systems has the potential to cause an evolutionary response in the life history of impacted organisms.

Hampton, S.E., and N.A. Friedenberg. 2001. Nocturnal increases in the use of near-surface water by pond animals. Hydrobiologia 477: 171-179
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We assessed diel animal habitat use in three shallow ponds, using unbaited funnel traps, a large column sampler, and sweep net collections in the upper stratum (0–0.3 m) of littoral and open habitats. In all three ponds, more animals were caught at night than during the day, indicating that use of near-surface waters was greatest at night, particularly in the fishless ponds. All methods yielded similar patterns. Our results demonstrate that nocturnal observations of pond animals are necessary to describe their ecology, even in fishless ponds where diel differences in habitat use or behavior might not be anticipated.

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