Nicholas A. Friedenberg
Martinez, J.C., M.A. Caprio,
and N.A. Friedenberg. 2018. Density dependence
and growth rate: evolutionary effects on resistance development
to Bt (Bacillus thuringiensis). Journal of Economic Entomology
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 Berliner (Bacillales:
Bacillaceae)), 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 timing and strength
of density dependence interacted 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 benefits 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 postselection densities, decreasing its strength
could increase durability. The strength of density dependence could
affect durability of both single traits and pyramids, but its influence
depended on the timing of density dependence and 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 timing and strength of interactions causing density
dependent mortality can all affect durability, also highlights
the need for ecologically integrated approaches to IRM research.
Monzon, J.D., and N.A.
2018. Metrics of population status for long-lived territorial birds:
a case study of golden eagle demography. Biological Conservation
The development of "snapshot" metrics that can serve
as reliable diagnostic tools for rapidly assessing population status
has great appeal. We used stochastic simulation moeling and recursive
partitioning to evaluate the reliability of two proposed snapshot
metrics in territorial raptors: the floater/breeder ratio and the
rate of nest occupancy by immature subadults. A demographic model,
parameterized with field data from an intensively studies population
of golden eagle (Aquila chrysaetos), showed that neither
metric, along or together, is a good indicator of population status.
However, one snaptshot metric, the floater/breeder ratio/ can help
predict the risk of population decline when considered in combination
with other information about the population or environment that
may be quickly appraised in the field or literature. Specifically,
qualitative knowledge of adult survival and whether the population
is limited by prey or habitat availability can help with rapid
risk assessment of raptor populations.
J.J. Hoover, K. Boysen, and K.J. Killgore. 2018. Estimating abundance
without recaptures of marked pallid sturgeon in the Mississippi
River. Conservation Biology DOI:
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
during mountain pine beetle outbreaks. Journal of Animal Ecology 87:73-86.
reprint from author
- 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
(low beetle densities), infestations are characterized by apparently
random spots (of 1-10 trees).
- 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.
- 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,
calculated yearly maps of travel time to previous beetle
beetle spots were sorted by travel time and compared with
predictions. Random eruption of locally endemic populations was
artificially-seeded spots. We also evaluated the relationship
between number of new spots and size of the perimeter of
- Spot distributions conformed strongly to predicted
power-law behavior. The spatially random eruption hypothesis
to be highly improbable. Spot numbers grew consistently
of previously infested area, suggesting that MPB spread
long distances from the boundary via spots following an inverse
- The Allee effect in MPB therefore accelerates,
rather than limits, invasion rates, contributing to recent
mortality in western North America.
and C. Foley. 2016. Defining protection of endangered
species from an integrated multispecies perspective. Technical
Report 3002008418. Electric Power Research Institute, Palo Alto,
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.
and K.T. Shoemaker. 2014. RAMAS IRM
version 2.0: Software for risk-based durability assessment. Applied
Biomathematics, Setauket, NY
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.
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.
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
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
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
preventing population risks at flood control diversions.
Dennehy, J.J., N.A.
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.
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,
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
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
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
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
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.
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
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
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
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.
R.D. Holt, P.E. Turner. 2006. Viral ecology and the maintenance
of novel host use. American Naturalist 167: 429-439
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.
2003. Determinism in a transient assemblage: the roles of dispersal
and local competition. American Naturalist 162: 586-596
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.
2003. Experimental evolution of dispersal in spatiotemporally variable
microcosms. Ecology Letters 6: 953-959
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
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
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