Julie Schram, Ph.D. is Assistant Professor of Animal Biology

Recent Submissions

  • Macroalgal input into the coastal food web along a gradient of seasonal sea ice cover along the Western Antarctic Peninsula

    Iken, Katrin; Amsler, Charles D.; Gorman, Kristen B.; Klein, Andrew G.; Galloway, Aaron W. E.; Amsler, Margaret O.; Heiser, Sabrina; Whippo, Ross; Lowe, Alexander T.; Schram, Julie; et al. (Inter-Research, 2023-09-07)
    Coastal food webs that are supported by multiple primary producer sources are considered to be more stable against perturbations. Here, we investigated how declining macroalgal abundance and diversity might influence coastal food web structure along an annual sea ice cover gradient along the Western Antarctic Peninsula (WAP). The most common benthic invertebrate consumers, macroalgae, and surface particulate organic matter were collected at 15 stations along the WAP. Stable carbon and nitrogen isotope values of primary producers changed negligibly in relation to the sea ice cover gradient, while isotope values of most invertebrate feeding groups increased with higher sea ice cover, although at low explanatory power. Food web length became shorter and consumer trophic niche width smaller in regions with higher sea ice cover. Changes in food web structure were mostly associated with shifts in trophic position of lower trophic levels. Food web structure in higher ice-covered regions resembled that of more generalist feeders with a loss of specialist species, concurrent with an increased reliance on a more reworked detrital food source. These results suggest that a number of benthic invertebrates are able to adjust to differences in basal energy sources. Conversely, these food webs dominated by generalist feeders are likely less efficient in energy transfer, which can create less-stable systems with lower adaptive capacity to disturbance. The predicted sea ice loss along the WAP may ultimately lead to a longer food web with higher macroalgal abundance, more specialist species, and wider consumer trophic niches in the currently more ice-covered regions.
  • Juvenile Dungeness crab foraging behavior and lipid composition is altered more by food quantity than seawater pH in a multi-stressor experiment

    Schram, Julie; Hayes, Hannah G.; Street, Erica; Thompson, Natalie; Yoshioka, Reyn M.; Galloway, Aaron W. E. (Elsevier, 2023-06)
    Increases in atmospheric, anthropogenic carbon are driving reductions in seawater pH, a process referred to as ocean acidification. Reduced seawater pH can influence behavior of marine animals, but little is currently known about how juvenile crustaceans will respond. We conducted lab experiments to improve our understanding of the consequences of pH exposure and food quantity on juvenile Dungeness crab (Metacarcinus magister, (Dana, 1852)) behavior and nutritional condition. To understand the foraging and pH sensing behavior of juvenile crab, and how this interacts with their nutritional status, we exposed recently settled second instar juveniles to either ambient pH or reduced pH for 42-d, crossed with either a ‘maintenance’- or low-quantity ‘challenge’ diet treatment. After the experimental exposure period, we introduced crab into foraging and sensing pH behavior experiments. In the foraging experiment, we placed crab in a behavior arena with unidirectional flow, where we measured the food discovery time and time allocation of activities in 300-s trials for all individual crab. Food quantity and pH exposure influenced both the speed with which juvenile crab identified and allocation of activities but there was no interactive effect of experimental factors. For our pH sensing experiment, we used a two-current flume plumbed with both ambient and reduced pH seawater. This flow-through flume provided a choice between the pH treatment waters and allowed us to measure the amount of time individuals spent on either side of the arena in 300-s trials. There was no effect of prior diet or pH exposure on the amount of time juvenile crab spent in either seawater pH condition. In addition to the behavior trials, we evaluated crab nutritional condition by quantifying the total lipid content of whole-body tissues and fatty acid profile composition of juvenile crab fed either the maintenance or low-quantity diet during the experimental pH exposure period. The proportional fatty acid profiles differed for crab based on their diet and pH exposure, with no interactive effects. However, we did not detect differences in the concentrations of key summary categories of fatty acids (e.g., saturated, monounsaturated, or polyunsaturated) based on pH exposure. Our results indicate that reduced food availability has a greater impact on juvenile Dungeness crab foraging behavior and nutritional condition than reduced seawater pH exposure representing the 0.3 pH unit decrease predicted by 2100.
  • Strong correlations of sea ice cover with macroalgal cover along the Antarctic Peninsula: Ramifications for present and future benthic communities

    Amsler, Charles D.; Amsler, Margaret O.; Klein, Andrew; Galloway, Aaron W. E.; Iken, Katrin; McClintock, James B.; Heiser, Sabrina; Lowe, Alex T.; Schram, Julie; Whippo, Ross (University of California Press, 2023-11)
    Macroalgal forests dominate shallow hard bottom areas along the northern portion of the Western Antarctic Peninsula (WAP). Macroalgal biomass and diversity are known to be dramatically lower in the southern WAP and at similar latitudes around Antarctica, but few reports detail the distributions of macroalgae or associated macroinvertebrates in the central WAP. We used satellite imagery to identify 14 sites differing in sea ice coverage but similar in terms of turbidity along the central WAP. Fleshy macroalgal cover was strongly, negatively correlated with ice concentration, but there was no significant correlation between macroinvertebrate cover and sea ice. Overall community (all organisms) diversity correlated negatively with sea ice concentration and positively with fleshy macroalgal cover, which ranged from around zero at high ice sites to 80% at the lowest ice sites. Nonparametric, multivariate analyses resulted in clustering of macroalgal assemblages across most of the northern sites of the study area, although they differed greatly with respect to macroalgal percent cover and diversity. Analyses of the overall communities resulted in three site clusters corresponding to high, medium, and low fleshy macroalgal cover. At most northern sites, macroalgal cover was similar across depths, but macroalgal and macroinvertebrate distributions suggested increasing effects of ice scour in shallower depths towards the south. Hindcast projections based on correlations of ice and macroalgal cover data suggest that macroalgal cover at many sites could have been varying substantially over the past 40 years. Similarly, based on predicted likely sea ice decreases by 2100, projected increases in macroalgal cover at sites that currently have high ice cover and low macroalgal cover are substantial, often with only a future 15% decrease in sea ice. Such changes would have important ramifications to future benthic communities and to understanding how Antarctic macroalgae may contribute to future blue carbon sequestration.
  • Effects of spatially heterogeneous lakeside development on nearshore biotic communities in a large, deep, oligotrophic lake

    Meyer, Michael F.; Ozersky, Ted; Woo, Kara H.; Shchapov, Kirill; Galloway, Aaron W. E.; Schram, Julie B.; Rosi, Emma J.; Snow, Daniel D.; Timofeyev, Maxim A.; Karnaukhov, Dmitry Yu.; et al. (Association for the Sciences of Limnology and Oceanography, 2022)
    Sewage released from lakeside development can reshape ecological communities. Nearshore periphyton can rapidly assimilate sewage-associated nutrients, leading to increases of filamentous algal abundance, thus altering both food abundance and quality for grazers. In Lake Baikal, a large, ultra-oligotrophic, remote lake in Siberia, filamentous algal abundance has increased near lakeside developments, and localized sewage input is the suspected cause. These shifts are of particular interest in Lake Baikal, where endemic littoral biodiversity is high, lakeside settlements are mostly small, tourism is relatively high ( 1.2 million visitors annually), and settlements are separated by large tracts of undisturbed shoreline, enabling investigation of heterogeneity and gradients of disturbance. We surveyed sites along 40 km of Baikal’s southwestern shore for sewage indicators—pharmaceuticals and personal care products (PPCPs) and microplastics—as well as periphyton and macroinvertebrate abundance and indicators of food web structure (stable isotopes and fatty acids). Summed PPCP concentrations were spatially related to lakeside development. As predicted, lakeside development was associated with more filamentous algae and lower abundance of sewage-sensitive mollusks. Periphyton and macroinvertebrate stable isotopes and essential fatty acids suggested that food web structure otherwise remained similar across sites; yet, the invariance of amphipod fatty acid composition, relative to periphyton, suggested that grazers adjust behavior or metabolism to compensate for different periphyton assemblages. Our results demonstrate that even low levels of human disturbance can result in spatial heterogeneity of nearshore ecological responses, with potential for changing trophic interactions that propagate through the food web.
  • Evolution of marine organisms under climate change at different levels of biological organisation.

    Harvey, Ben P.; Al-Janabi, Balsam; Broszeit, Stefanie; Cioffi, Rebekah; Kumar, Amit; Aranguren-Gassi, Maria; Bailey, Allison; Green, Leon; Gsottbauer, Carina M.; Hall, Emilie F.; et al. (Multidisciplinary Digital Publishing Institute, 2014)
    Research to date has suggested that both individual marine species and ecological processes are expected to exhibit diverse responses to the environmental effects of climate change. Evolutionary responses can occur on rapid (ecological) timescales, and yet studies typically do not consider the role that adaptive evolution will play in modulating biological responses to climate change. Investigations into such responses have typically been focused at particular biological levels (e.g., cellular, population, community), often lacking interactions among levels. Since all levels of biological organisation are sensitive to global climate change, there is a need to elucidate how different processes and hierarchical interactions will influence species fitness. Therefore, predicting the responses of communities and populations to global change will require multidisciplinary efforts across multiple levels of hierarchy, from the genetic and cellular to communities and ecosystems. Eventually, this may allow us to establish the role that acclimatisation and adaptation will play in determining marine community structures in future scenarios.
  • Seawater acidification more than warming presents a challenge for two Antarctic macroalgal-associated amphipods

    Schram, Julie B.; Schoenrock, Kathryn M.; McClintock, James B.; Amsler, Charles D.; Angus, Robert A. (Inter-Research, 2016-07-08)
    Elevated atmospheric pCO2 concentrations are triggering seawater pH reductions and seawater temperature increases along the western Antarctic Peninsula (WAP). These factors in combination have the potential to influence organisms in an antagonistic, additive, or synergistic manner. The amphipods Gondogeneia antarctica and Paradexamine fissicauda represent prominent members of macroalgal-associated mesograzer assemblages of the WAP. Our primary objective was to investigate amphipod behavioral and physiological responses to reduced seawater pH and elevated temperature to evaluate potential cascading ecological impacts. For 90 d, amphipods were exposed to combinations of seawater conditions based on present ambient (pH 8.0, 1.5°C) and predicted end-of-century conditions (pH 7.6, 3.5°C). We recorded survival, molt frequency, and macroalgal consumption rates as well as change in wet mass and proximate body composition (protein and lipid). Survival for both species declined significantly at reduced pH and co-varied with molt frequency. Consumption rates in G. antarctica were significantly higher at reduced pH and there was an additive pH−temperature effect on consumption rates in P. fissicauda. Body mass was reduced for G. antarctica at elevated temperature, but there was no significant effect of pH or temperature on body mass in P. fissicauda. Exposure to the pH or temperature levels tested did not induce significant changes in whole body biochemical composition of G. antarctica, but exposure to elevated temperature resulted in a significant increase in whole body protein content of P. fissicauda. Our study indicates that while elevated temperature causes sub-lethal impacts on both species of amphipods, reduced pH causes significant mortality.
  • Ocean warming and acidification alter Antarctic macroalgal biochemical composition but not amphipod grazer feeding preferences

    Schram, Julie B.; Schoenrock, Kathryn M.; McClintock, James B.; Amsler1, Charles D.; Angus, Robert A. (Inter-Research, 2017-10-13)
    Increased anthropogenic atmospheric CO2 concentrations have resulted in ocean warming and alterations in ocean carbonate chemistry, decreasing seawater pH (ocean acidification). The combination of ocean warming and acidification (OWA) may alter trophic interactions in marine benthic communities along the western Antarctic Peninsula (WAP). Abundant and diverse macroalgae–grazer assemblages, dominated by macroalgae (e.g. chemically defended Desmarestia anceps and D. menziesii) and gammarid amphipods (e.g. Gondogeneia antarctica), occur on the nearshore benthos along the WAP. In the present study, the amphipod G. antarctica and macroalgae D. anceps and D. menziesii were exposed for 39 and 79 d, respectively, to combinations of current and predicted near-future temperature (1.5 and 3.5°C, respectively) and pH (8.0 and 7.6, respectively). Protein and lipid levels of macroalgal tissues were quantified, and 5-way choice amphipod feeding assays were performed with lyophilized macroalgal tissues collected at time zero and following exposure to the 4 temperature-pH treatments. For D. anceps, we found a significant interactive temperature-pH effect on lipid levels and significantly lower protein levels at reduced pH. In contrast, tissues of D. menziesii exhibited significantly greater lipid levels after exposure to reduced pH, but there was no temperature effect on lipid or protein levels. Despite shifts in macroalgal biochemical composition, there were no changes in amphipod feeding preferences. Our results indicate that despite altered macroalgal nutritional quality under OWA, both macroalgae retained their ability to deter amphipod feeding. This deterrent capacity could become an important contributor to net community resistance of macroalgae−mesograzer assemblages of the WAP to predicted OWA.
  • Trophic Transfer of Macroalgal Fatty Acids in Two Urchin Species: Digestion, Egestion, and Tissue Building

    Schram, Julie B.; Kobelt, Julia N.; Dethier, Megan N.; Galloway, Aaron W. E. (Frontiers in Ecology and Evolution, 2018-06-19)
    Sea urchins are ecosystem engineers of nearshore benthic communities because of their influence on the abundance and distribution of macroalgal species. Urchins are notoriously inefficient in assimilation of their macroalgal diets, so their fecal production can provide a nutritional subsidy to benthic consumers that cannot capture and handle large macroalgae. We studied the assimilation of macroalgal diets by urchins by analyzing the profiles of trophic biomarkers such as fatty acids (FAs). We tracked macroalgal diet assimilation in both Strongylocentrotus droebachiensis and S. purpuratus. Juvenile S. droebachiensis and adult S. purpuratus were maintained for 180 and 70 days, respectively, on one of three monoculture diets from three algal phyla: Nereocystis luetkeana, Pyropia sp., or Ulva sp. We then analyzed FA profiles of the macroalgal tissue fed to urchins as well as urchin gonad, gut, digesta, and egesta (feces) to directly evaluate trophic modification and compare nutritional quality of urchin food sources, urchin tissues, and fecal subsidies. In the S. purpuratus assay, there were significantly more total lipids in the digesta and egesta than in the algae consumed. The FA profiles of urchin tissues differed among urchin species, all diets, and tissue types. Despite these differences, we observed similar patterns in the relationships between the urchin and macroalgal tissues for both species. Egesta produced by urchins fed each of the three diets were depleted with respect to the concentration of important long chain polyunsaturated fatty acids (LCPUFAs), but did not differ significantly from the source alga consumed. Both urchin species were shown to synthesize and selectively retain both the precursor and resulting LCPUFAs involved in the synthesis of the LCPUFAs 20:4ω6 and 20:5ω3. S. droebachiensis and S. purpuratus exhibited consistent patterns in the respective depletion and retention of precursor FAs and resulting LCPUFAs of Pyropia and Ulva tissues, suggesting species level control of macroalgal digestion or differential tissue processing by gut microbiota. For both S. droebachiensis and S. purpuratus, macroalgal diet was a surprisingly strong driver of urchin tissue fatty acids; this indicates the potential of fatty acids for future quantitative trophic estimates of urchin assimilation of algal phyla in natural settings.
  • The Purple Sea Urchin Strongylocentrotus purpuratus Demonstrates a Compartmentalization of Gut Bacterial Microbiota, Predictive Functional Attributes, and Taxonomic Co-Occurrence

    Hakim, Joseph A.; Schram, Julie B.; Galloway, Aaron W. E.; Morrow, Casey D.; Crowley, Michael R.; Watts, Stephen A.; Bej, Asim K. (Multidisciplinary Digital Publishing Institute, 2019-01-26)
    The sea urchin Strongylocentrotus purpuratus (order Camarodonta, family Strongylocentrotidae) can be found dominating low intertidal pool biomass on the southern coast of Oregon, USA. In this case study, three adult sea urchins were collected from their shared intertidal pool, and the bacteriome of their pharynx, gut tissue, and gut digesta, including their tide pool water and algae, was determined using targeted high-throughput sequencing (HTS) of the 16S rRNA genes and bioinformatics tools. Overall, the gut tissue demonstrated Arcobacter and Sulfurimonas (Epsilonproteobacteria) to be abundant, whereas the gut digesta was dominated by Psychromonas (Gammaproteobacteria), Propionigenium (Fusobacteria), and Flavobacteriales (Bacteroidetes). Alpha and beta diversity analyses indicated low species richness and distinct microbial communities comprising the gut tissue and digesta, while the pharynx tissue had higher richness, more closely resembling the water microbiota. Predicted functional profiles showed Kyoto Encyclopedia of Genes and Genomes (KEGG) Level-2 categories of energy metabolism, membrane transport, cell motility, and signal transduction in the gut tissue, and the gut digesta represented amino acid, carbohydrate, vitamin and cofactor metabolisms, and replication and repair. Co-occurrence network analysis showed the potential relationships and key taxa, such as the highly abundant Arcobacter and Propionigenium, influencing population patterns and taxonomic organization between the gut tissue and digesta. These results demonstrate a trend of microbial community integration, allocation, predicted metabolic roles, and taxonomic co-occurrence patterns in the S. purpuratus gut ecosystem.
  • Eelgrass pathogen Labyrinthula zosterae synthesizes essential fatty acids

    Yoshioka, R. M.; Schram, Julie B.; Galloway, Aaron W. E. (Inter-Research, 2019-07-25)
    Negative consequences of parasites and disease on hosts are usually better understood than their multifaceted ecosystem effects. The pathogen Labyrinthula zosterae (Lz) causes eelgrass wasting disease but has relatives that produce large quantities of nutritionally valuable long-chain polyunsaturated fatty acids (LCPUFA) such as docosahexaenoic acid (DHA). Here we quantify the fatty acids (FA) of Lz cultured on artificial media, eelgrass-based media, and eelgrass segments to investigate whether Lz may similarly produce LCPUFA. We also assess whether fieldcollected lesions show similar FA patterns to laboratory-inoculated eelgrass. We find that Lz produces DHA as its dominant FA along with other essential FA on both artificial and eelgrass-based media. DHA content was greater in both laboratory-inoculated and field-collected diseased eelgrass relative to their respective controls. If Lz’s production scales in situ, it may present an unrecognized source of LCPUFA in eelgrass ecosystems.
  • Ghost Factors of Laboratory Carbonate Chemistry Are Haunting Our Experiments

    Galloway, Aaron W. E.; Dassow, G. Von; Schram, Julie B.; Klinger, T.; Hill, T. M.; Lowe, A. T.; Chan, F.; Yoshioka, R. M.; Kroeker, K. J. (The University of Chicago, 2020-10-23)
    For many historical and contemporary experimental studies in marine biology, seawater carbonate chemistry remains a ghost factor, an uncontrolled, unmeasured, and often dynamic variable affecting experimental organisms or the treatments to which investigators subject them. We highlight how environmental variability, such as seasonal upwelling and biological respiration, drive variation in seawater carbonate chemistry that can influence laboratory experiments in unintended ways and introduce a signal consistent with ocean acidification. As the impacts of carbonate chemistry on biochemical pathways that underlie growth, development, reproduction, and behavior become better understood, the hidden effects of this previously overlooked variable need to be acknowledged. Here we bring this emerging challenge to the attention of the wider community of experimental biologists who rely on access to organisms and water from marine and estuarine laboratories and who may benefit from explicit considerations of a growing literature on the pervasive effects of aquatic carbonate chemistry changes.
  • Sea otter effects on trophic structure of seagrass communities in southeast Alaska

    Raymond, Wendel W.; Schram, Julie B.; Eckert, Ginny L.; Galloway, Aaron W. E. (Inter-Research, 2021-09-16)
    Previous research in southeast Alaska on the effects of sea otters Enhydra lutris in seagrass Zostera marina communities identified many but not all of the trophic relationships that were predicted by a sea otter-mediated trophic cascade. To further resolve these trophic connections, we compared biomass, carbon (δ13C) and nitrogen (δ15N) stable isotope (SI), and fatty acid (FA) data from 16 taxa at 3 sites with high and 3 sites with low sea otter density (8.2 and 0.1 sea otters km−2, respectively). We found lower crab and clam biomass in the high sea otter region but did not detect a difference in biomass of other seagrass community taxa or the overall community isotopic niche space between sea otter regions. Only staghorn sculpin differed in δ13C between regions, and Fucus, sugar kelp, butter clams, dock shrimp, and shiner perch differed in δ15N. FA analysis indicated multivariate dissimilarity in 11 of the 15 conspecifics between sea otter regions. FA analysis found essential FAs, which consumers must obtain from their diet, including 20:5ω3 (EPA) and 22:6ω3 (DHA), were common in discriminating conspecifics between sea otter regions, suggesting differences in consumer diets. Further FA analysis indicated that many consumers rely on diverse diets, regardless of sea otter region, potentially buffering these consumers from sea otter-mediated changes to diet availability. While sea otters are major consumers in this system, further studies are needed to understand the mechanisms responsible for the differences in biomarkers between regions with and without sea otters
  • A unified dataset of colocated sewage pollution, periphyton, and benthic macroinvertebrate community and food web structure from Lake Baikal (Siberia)

    Meyer, Michael F.; Ozersky, Ted; Woo, Kara H.; Shchapov, Kirill; Galloway, Aaron W. E.; Schram, Julie B.; Snow, Daniel D.; Timofeyev, Maxim A.; Karnaukhov, Dmitry Yu.; Brousil, Matthew R.; et al. (Wiley Periodicals LLC, 2021)
    Sewage released from lakeside development can introduce nutrients and micropollutants that can restructure aquatic ecosystems. Lake Baikal, the world’s most ancient, biodiverse, and voluminous freshwater lake, has been experiencing localized sewage pollution from lakeside settlements. Nearby increasing filamentous algal abundance suggests benthic communities are responding to localized pollution. We surveyed 40-km of Lake Baikal’s southwestern shoreline from 19 to 23 August 2015 for sewage indicators, including pharmaceuticals, personal care products, and microplastics, with colocated periphyton, macroinvertebrate, stable isotope, and fatty acid samplings. The data are structured in a tidy format (a tabular arrangement familiar to limnologists) to encourage reuse. Unique identifiers corresponding to sampling locations are retained throughout all data files to facilitate interoperability among the dataset’s 150+ variables. For Lake Baikal studies, these data can support continued monitoring and research efforts. For global studies of lakes, these data can help characterize sewage prevalence and ecological consequences of anthropogenic disturbance across spatial scales.
  • Assessing prevalence and correlates of blue‑colored fesh in lingcod (Ophiodon elongatus) across their geographic range

    Galloway, Aaron W. E.; Beaudreau, Anne H.; Thomas, Michael D.; Basnett, Bonnie L.; Lam, Laurel S.; Hamilton, Scott L.; Andrews, Kelly S.; Schram, Julie B.; Watson, Jessica; Samhouri4, Jameal F. (Springer, 2021-08-17)
    Intraspecific variation in external and internal pigmentation is common among fishes and explained by a variety of biological and ecological factors. Blue-colored flesh in fishes is relatively rare but has been documented in some species of the sculpin, greenling, and perch families. Diet, starvation, photoprotection, and camouflage have all been suggested as proximate mechanisms driving blue flesh, but causal factors are poorly understood. We evaluated the relative importance of biological and spatial factors that could explain variation in blue coloration in 2021 lingcod (Ophiodon elongatus) captured across their range in the northeastern Pacific, from southeast Alaska to southern California. The probability of having blue flesh was highest for fish that were female, caught in shallower water, and smaller in body size. The incidence of blueness varied by region (4–25% of all fish) but was also confounded by differences in sex ratios of fish caught among regions. We analyzed the multivariate fatty acid composition of a subset of 175 fish from across the sampling range to test for differences in trophic biomarkers in blue lingcod. Lingcod fatty acid composition differed between regions and flesh colors but not between sexes. Blue-fleshed fish had lower concentrations of total fatty acids, 18:1ω-9, 16:1ω-7, 18:1ω-7, and ω-6 fatty acids, suggesting differences in energetics and energy storage in blue fish. While our data indicate potential links between diet and blue flesh in lingcod, important questions remain about the physiological mechanisms governing blueness and its biological consequences.