Publications by EEOB faculty June 1 - June 30

May 24, 2016
EEOB graphic 2016

The re-eutrophication of Lake Erie: Harmful algal blooms and hypoxia

Susan B. Watson, Carol Miller, George Arhonditsis, Gregory L. Boyer, Wayne Carmichael, Murray N. Charlton, Remegio Confesor, David C. Depew, Tomas O. Höök, Stuart A. Ludsin, Gerald Matisoff, Shawn P. McElmurry, Michael W. Murray, R. Peter Richards, Yerubandi R. Rao, Morgan M. Steffen, Steven W. Wilhelm. 2016. doi:10.1016/j.hal.2016.04.010


Lake Erie supplies drinking water to more than 11 million consumers, processes millions of gallons of wastewater, provides important species habitat and supports a substantial industrial sector, with >$50 billion annual income to tourism, recreational boating, shipping, fisheries, and other industries. These and other key ecosystem services are currently threatened by an excess supply of nutrients, manifested in particular by increases in the magnitude and extent of harmful planktonic and benthic algal blooms (HABs) and hypoxia. Widespread concern for this important international waterbody has been manifested in a strong focus of scientific and public material on the subject, and commitments for Canada-US remedial actions in recent agreements among Federal, Provincial and State agencies. This review provides a retrospective synthesis of past and current nutrient inputs, impairments by planktonic and benthic HABs and hypoxia, modelling and Best Management Practices in the Lake Erie basin. The results demonstrate that phosphorus reduction is of primary importance, but the effects of climate, nitrogen and other factors should also be considered in the context of adaptive management. Actions to reduce nutrient levels by targeted Best Management Practices will likely need to be tailored for soil types, topography, and farming practices.

Within-group relatedness is correlated with colony-level social structure and reproductive sharing in a social fish. 

Hellmann, J. K., Sovic, M. G., Gibbs, H. L., Reddon, A. R., O'Connor, C. M., Ligocki, I. Y., Marsh-Rollo, S., Balshine, S. and Hamilton, I. M. 2016. Mol Ecol. doi:10.1111/mec.13728


In group-living species, the degree of relatedness among group members often governs the extent of reproductive sharing, cooperation, and conflict within a group. Kinship among group members can be determined by the presence and location of neighboring groups, as these provide dispersal or mating opportunities that can dilute kinship among current group members. Here we assessed how within-group relatedness varies with the density and position of neighboring social groups in Neolamprologus pulcher, a colonial and group-living cichlid fish. We used restriction site-associated DNA sequencing (RADseq) methods to generate thousands of polymorphic SNPs. Relative to microsatellite data, RADseq data provided much smaller confidence intervals around relatedness estimates. These data allowed us to document novel patterns of relatedness in relation to colony-level social structure. First, the density of neighboring groups was negatively correlated with relatedness between subordinates and dominant females within a group, but no such patterns were observed between subordinates and dominant males. Second, subordinates at the colony edge were less related to dominant males in their group than subordinates in the colony center, suggesting a shorter breeding tenure for dominant males at the colony edge. Finally, subordinates who were closely related to their same-sex dominant were more likely to reproduce, supporting some restraint models of reproductive skew. Collectively, these results demonstrate that within-group relatedness is influenced by the broader social context, and variation between groups in the degree of relatedness between dominants and subordinates can be explained by both patterns of reproductive sharing and the nature of the social landscape.

Evaluating forest subcanopy response to moderate severity disturbance and contribution to ecosystem-level productivity and resilience

Robert T. Fahey, Ellen J. Stuart-Haëntjens, Christopher M. Gough, Aubrie De La Cruz, Elizabeth Stockton, Christoph S. Vogel, Peter S. Curtis. 2016. Forest Ecology and Management. 376:135–147. doi:10.1016/j.foreco.2016.06.001


North American temperate forests have functioned as a terrestrial carbon (C) sink for more than a century, but the future of this sink is highly uncertain as disturbance frequency increases and regrown forests approach maturity. The subcanopy is integral to the functional recovery of forests, supporting short-term resilience of primary production and longer-term shifts in tree species composition and diversity. However, the factors that contribute to variation in forest subcanopy response to disturbance are not well understood. In this study, we investigated subcanopy shifts in aboveground wood net primary productivity (ANPPw) and composition following experimental moderate severity disturbance emulating natural canopy mortality from age-related senescence. We assessed the importance of variation in disturbance severity, site fertility, and community composition on subcanopy disturbance response and contribution to total (canopy and subcanopy) ANPPw response. We also assessed the effect of the moderate severity disturbance on species composition and diversity, and competitive patterns within the subcanopy layer. Subcanopy aboveground biomass and ANPPw increased substantially relative to pre-disturbance levels by a factor of 1.4 and 22.7, respectively. The subcanopy (stems <8 cm DBH) made up a large component of overall (canopy plus subcanopy) post disturbance ANPPw (16.2%) and disturbance response (post-disturbance ANPPw/pre-disturbance ANPPw; 54.1%). Subcanopy ANPPw, subcanopy post-disturbance ANPPw response, and subcanopy contribution to total post-disturbance ANPPw response were all most strongly predicted by subcanopy community composition in combination with canopy composition and site fertility. Variation in disturbance severity was not a strong predictor of subcanopy ANPPw response to disturbance. Subcanopy compositional trends and growth patterns both indicate likely increased heterogeneity in canopy composition (greater β diversity) and a potential shift toward greater dominance by mid-tolerant Quercus rubra (northern red oak). Our results illustrate the importance of the subcanopy in the response of forest productivity to moderate severity disturbance and illustrate that composition of the subcanopy layer exerts a strong influence on the growth response both of the subcanopy and the forest as a whole. Our findings highlight the unique role of moderate severity disturbance, relative to more severe disturbances, in promoting biological and structural heterogeneity in forest ecosystems and favoring underrepresented mid-tolerant species.

Geographical variation in song phrases differs with their function in white-crowned sparrow song

Douglas A. Nelson. 2016. doi:10.1016/j.anbehav.2016.05.016


White-crowned sparrow songs are composed of phrase types with different functions. The whistle phrase alerts listeners or conveys species identity and is geographically invariant. The note complex and trill phrases identify individuals and dialects and vary geographically. Note complexes and trills have somewhat independent geographical distributions. The phrase types appear to develop along different pathways.

Population genetics of Penstemon albomarginatus (Plantaginaceae), a rare Mojave Desert species of conservation concern

Andrea D. Wolfe, Timothy Necamp, Susan Fassnacht, Paul Blischak, Laura Kubatko. 2016. DOI: 10.1007/s10592-016-0857-y


Penstemon albomarginatus is a psammophytic endemic of the Mojave Desert, found only in deep sand and dune habitats of San Bernardino County, California, Mohave County, Arizona, and Clark and Nye Counties in Nevada. We used six microsatellite loci to assess genetic differentiation and diversity for 228 individuals across the 12 known populations of this rare species. A slight heterozygote deficiency was found in two populations, but most populations show no signs of inbreeding. Results show a geographic pattern of northern populations being more closely related to one another compared to all other geographic regions. Genetic diversity was greatest in the southern populations, with decreasing amounts of diversity observed with latitude. In general, the geographic pattern of genetic diversity among all populations suggests a post-glacial dispersal from south-to-north. Our results are discussed in the framework of anthropogenic pressures on deep sand habitats of the Mojave Desert.

Molecular Physiology of Mosquito Diapause

D.L. Denlinger, P.A. Armbruster. 2016. doi:10.1016/bs.aiip.2016.05.002


The dormant state of diapause is exploited by numerous mosquito species to survive seasonal periods of environmental stress. We discuss embryonic, larval and adult diapauses in mosquitoes and probe the molecular and physiological distinctions that comprise the diapause phenotype. Diapause evokes diverse and unique attributes including behavioural changes, arrested development, enhanced stress tolerance, fat accumulation and suppressed metabolic rates. Like most insects, mosquitoes in temperate latitudes precisely monitor daylength as a cue for diapause initiation. We examine the role of circadian clock genes in this response and trace downstream hormonal pathways involved in the diapause response. Insulin and the FOXO transcription factor signalling pathways appear to be keys for generating the diapause phenotype in adult females of Culex pipiens and perhaps other species. Elucidating the molecular regulation of diapause-associated physiology may provide a basis to identify novel targets for the control of mosquito vectors.

The cutaneous lipid composition of bat wing and tail membranes: a case of convergent evolution with birds

Miriam Ben-Hamo, Agustí Muñoz-Garcia, Paloma Larrain, Berry Pinshow, Carmi Korine, Joseph B. Williams. 2016. DOI: 10.1098/rspb.2016.0636


The water vapour permeability barrier of mammals and birds resides in the stratum corneum (SC), the outermost layer of the epidermis. The molar ratio and molecular arrangement of lipid classes in the SC determine the integrity of this barrier. Increased chain length and polarity of ceramides, the most abundant lipid class in mammalian SC, contribute to tighter packing and thus to reduced cutaneous evaporative water loss (CEWL). However, tighter lipid packing also causes low SC hydration, making it brittle, whereas high hydration softens the skin at the cost of increasing CEWL. Cerebrosides are not present in the mammalian SC; their pathological accumulation occurs in Gaucher's disease, which leads to a dramatic increase in CEWL. However, cerebrosides occur normally in the SC of birds. We tested the hypothesis that cerebrosides are also present in the SC of bats, because they are probably necessary to confer pliability to the skin, a quality needed for flight. We examined the SC lipid composition of four sympatric bat species and found that, as in birds, their SC has substantial cerebroside contents, not associated with a pathological state, indicating convergent evolution between bats and birds.
Changes in histone acetylation as potential mediators of pupal diapause in the flesh fly, Sarcophaga bullata

J.A. Reynolds, Robin Bautista-Jimenez, D.L. Denlinger. 2016. doi:10.1016/j.ibmb.2016.06.012


The growing appreciation that epigenetic processes are integral to the responses of many organisms to changes in the environment suggests a possible role for epigenetics in coordination of insect diapause. The results we present suggest that histone modification may be one type of epigenetic process that contributes to regulation of pupal diapause in the flesh fly, Sarcophaga bullata. Reduction in total histone H3 acetylation in diapausing pupae, shifts in mRNA expression profiles of genes encoding histone acetyltransferase (HAT) and histone deacetylase (HDAC) in pre-diapause, diapause and post-diapause flies compared to their nondiapause counterparts, and alterations in HDAC enzyme activity during and post-diapause lend support to the hypothesis that this specific type of histone modification is involved in regulating diapause programming, maintenance, and termination. Transcription of genes encoding HDAC1, HDAC3, HDAC6, and Sirtuin2 were all upregulated in photosensitive first instar larvae programmed to enter pupal diapause, suggesting that histone deacetylation may be linked to the early decision to enter diapause. A 50% reduction in transcription of hdac3 and a corresponding 30% reduction in HDAC activity during diapause suggest that removal of acetyl groups from histones primarily occurs prior to diapause entry and that further histone deacetylation is not necessary to maintain diapause. Transcription of the HDAC genes was quickly elevated when diapause was terminated, followed by an increase in enzyme activity after a short delay. A maternal effect operating in these flies prevents pupal diapause in progeny whose mothers experienced pupal diapause, even if the progeny are reared in strong diapause-inducing short-day conditions. Such nondiapausing pupae had HDAC transcription profiles nearly identical to the profiles seen in nondiapausing pupae generated under a long-day photoperiod. Together, these results provide consistent evidence for histone acetylation and deacetylation as regulators of this insect's developmental trajectory.

Thinking outside of the lake: Can controls on nutrient inputs into Lake Erie benefit stream conservation in its watershed?

S. Conor Keitzer, Stuart A. Ludsin, Scott P. Sowa, Gust Annis, Jeff G. Arnold, Prasad Daggupati, August M. Froehlich, Matt E. Herbert, Mari-Vaughn V. Johnson, Anthony M. Sasson, Haw Yen, Mike J. White, Charles A. Rewa. 2016. doi:10.1016/j.jglr.2016.05.012


Investment in agricultural conservation practices (CPs) to address Lake Erie's re-eutrophication may offer benefits that extend beyond the lake, such as improved habitat conditions for fish communities throughout the watershed. If such conditions are not explicitly considered in Lake Erie nutrient management strategies, however, this opportunity might be missed. Herein, we quantify the potential for common CPs that will be used to meet nutrient management goals for Lake Erie to simultaneously improve stream biological conditions throughout the western Lake Erie basin (WLEB) watershed. To do so, we linked a high-resolution watershed-hydrology model to predictive biological models in a conservation scenario framework. Our modeling simulations showed that the implementation of CPs on farm acres in critical and moderate need of treatment, representing nearly half of the watershed, would be needed to reduce spring/early summer total phosphorus loads from the WLEB watershed to acceptable levels. This widespread CP implementation also would improve potential stream biological conditions in > 11,000 km of streams and reduce the percentage of streams where water quality is limiting biological conditions, from 31% to 20%. Despite these improvements, we found that even with additional treatment of acres in low need of CPs, degraded water quality conditions would limit biological conditions in > 3200 stream km. Thus, while we expect CPs to play an important role in mitigating eutrophication problems in the Lake Erie ecosystem, additional strategies and emerging technologies appear necessary to fully reduce water quality limitation throughout the watershed.