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The landscape theory of food web architecture (LTFWA) describes relationships among body size, trophic position, mobility, and energy channels that serve to couple heterogenous habitats, which in turn promotes long-term system stability. However, empirical tests of the LTFWA are rare and support differs among terrestrial, freshwater, and marine systems. Further, it is unclear whether the theory applies in highly altered ecosystems dominated by introduced species such as the Laurentian Great Lakes. Here, we provide an empirical test of the LTFWA by relating body size, trophic position, and the coupling of different energy channels using stable isotope data from species throughout the Lake Michigan food web. We found that body size was positively related to trophic position, but for a given trophic position, organisms predominately supported by pelagic energy had smaller body sizes than organisms predominately supported by nearshore benthic energy. We also found a hump-shaped trophic relationship in the food web where there is a gradual increase in the coupling of pelagic and nearshore energy channels with larger body sizes as well as higher trophic positions. This highlights the important role of body size and connectivity among habitats in structuring food webs. However, important deviations from expectations are suggestive of how species introductions and other anthropogenic impacts can affect food web structure in large lakes. First, native top predators appear to be flexible couplers that may provide food web resilience, whereas introduced top predators may confer less stability when they specialize on a single energy pathway. Second, some smaller bodied prey fish and invertebrates, in addition to mobile predators, coupled energy from pelagic and nearshore energy channels, which suggests that some prey species may also be important integrators of energy pathways in the system. We conclude that patterns predicted by the LTFWA are present in the face of species introductions and other anthropogenic stressors to a degree, but time-series evaluations are needed to fully understand the mechanisms that promote stability.

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The restoration of the once abundant Cisco (Coregonus artedi) is a management interest across the Laurentian Great Lakes. To inform the restoration, we (1) described historical distributions of Cisco and (2) explored whether non-indigenous Rainbow Smelt (Osmerus mordax) and Alewife (Alosa pseudoharengus) played a role in the decline of Cisco populations across the upper Great Lakes (i.e., Lakes Superior, Michigan, and Huron). Our source data were collected from fishery-independent surveys conducted by the U.S. Fish and Wildlife Service's research vessel R/V Cisco in 1952-1962. By analyzing data collected by gill-net surveys, we confirmed the importance of embayment and shallow-water habitats to Cisco. We found that Cisco was abundant in Whitefish Bay and Keweenaw Bay, Lake Superior, and in Green Bay, Lake Michigan, but we also found a sign of Cisco extirpation in Saginaw Bay, Lake Huron. Our results also showed that Ciscoes generally stayed in waters <80 m in bottom depth throughout the year. However, a substantial number of Ciscoes stayed in very deep waters (>150 m in bottom depth) in summer and fall in Lake Michigan, although we cannot exclude the possibility that these Ciscoes had hybridized with the other Coregonus species. By comparing complementary data collected from bottom-trawl surveys, we concluded that the spatiotemporal overlap between Rainbow Smelt and Cisco likely occurred across the upper Great Lakes throughout 1952-1962. These data were consistent with the hypothesis that Rainbow Smelt played a role in the decline of Cisco populations across the upper Great Lakes in the period. We also found that the spatiotemporal overlap between Alewife and Cisco likely occurred only in Saginaw Bay in fall 1956 and in Lake Michigan after 1960. Thus, any potential recovery of Cisco after the 1950s could have been inhibited by Alewife in Lakes Michigan and Huron.

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The larval stage of invasive Dreissena spp. mussels (i.e., veligers) are understudied despite their seasonal numerical dominance among plankton. We report the spring and summer veliger densities and size structure across the main basin, North Channel, and Georgian Bay of Lake Huron, and seek to explain spatiotemporal variation. Monthly sampling was conducted at 9 transects and up to 3 sites per transect from spring through summer 2017. Veliger densities peaked in June and July, and we found comparable densities and biomasses of veligers between basins, despite differences in density of juvenile and adult mussels across these regions. Using a generalized additive model to explain variations in veliger density, we found that temperature, chlorophyll a, and nitrates/nitrites were most important. We generated an index of veliger attrition based on size distributions that revealed a higher rate of attrition in the North Channel than the rest of the lake. A logistic model indicated a threshold calcium concentration of around 22 mg/L was necessary for veligers to survive to larger sizes and recruit to their juvenile and benthic adult life stages. Improved understanding of factors that regulate the production and survival of Dreissena veligers will improve the ability of managers to assess future invasion threats as well as explore potential control options.

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Species introductions provide opportunities to quantify rates and patterns of evolutionary change in response to novel environments. Alewives (Alosa pseudoharengus) are native to the East Coast of North America where they ascend coastal rivers to spawn in lakes and then return to the ocean. Some populations have become landlocked within the last 350 years and diverged phenotypically from their ancestral marine population. More recently, alewives were introduced to the Laurentian Great Lakes (~150 years ago), but these populations have not been compared to East Coast anadromous and landlocked populations. We quantified 95 years of evolution in foraging traits and overall body shape of Great Lakes alewives and compared patterns of phenotypic evolution of Great Lakes alewives to East Coast anadromous and landlocked populations. Our results suggest that gill raker spacing in Great Lakes alewives has evolved in a dynamic pattern that is consistent with responses to strong but intermittent eco-evolutionary feedbacks with zooplankton size. Following their initial colonization of Lakes Ontario and Michigan, dense alewife populations likely depleted large-bodied zooplankton, which drove a decrease in alewife gill raker spacing. However, the introduction of large, non-native zooplankton to the Great Lakes in later decades resulted in an increase in gill raker spacing, and present-day Great Lakes alewives have gill raker spacing patterns that are similar to the ancestral East Coast anadromous population. Conversely, contemporary Great Lakes alewife populations possess a gape width consistent with East Coast landlocked populations. Body shape showed remarkable parallel evolution with East Coast landlocked populations, likely due to a shared response to the loss of long-distance movement or migrations. Our results suggest the colonization of a new environment and cessation of migration can result in rapid parallel evolution in some traits, but contingency also plays a role, and a dynamic ecosystem can also yield novel trait combinations.

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Globally, our knowledge on lake fisheries is still limited despite their importance to food security and livelihoods. Here we show that fish catches can respond either positively or negatively to climate and land-use changes, by analyzing time-series data (1970-2014) for 31 lakes across five continents. We find that effects of a climate or land-use driver (e.g., air temperature) on lake environment could be relatively consistent in directions, but consequential changes in a lake-environmental factor (e.g., water temperature) could result in either increases or decreases in fish catch in a given lake. A subsequent correlation analysis indicates that reductions in fish catch was less likely to occur in response to potential climate and land-use changes if a lake is located in a region with greater access to clean water. This finding suggests that adequate investments for water-quality protection and water-use efficiency can provide additional benefits to lake fisheries and food security.

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With the global-scale loss of biodiversity, current restoration programs have been often required as part of conservation plans for species richness and ecosystem integrity. The restoration of pelagic-oriented cisco (Coregonus artedi) has been an interest of Lake Michigan managers because it may increase the diversity and resilience of the fish assemblages and conserve the integrity of the ecosystems in a changing environment. To inform restoration, we described historical habitat use of cisco by analyzing a unique fishery-independent dataset collected in 1930-1932 by the U.S. Bureau of Fisheries' first research vessel Fulmar and a commercial catch dataset reported by the State of Michigan in the same period, both based on gear fished on the bottom. Our results confirmed that the two major embayments, Green Bay and Grand Traverse Bay, were important habitats for cisco and suggest that the Bays were capable of supporting cisco to complete its entire life cycle in the early 20th century as there was no lack of summer feeding and fall spawning habitats. Seasonally, our results showed that cisco stayed in nearshore waters in spring, migrated to offshore waters in summer, and then migrated back to nearshore waters in fall. The results also suggest that in summer, most ciscoes were in waters with bottom depths of 20-70 m, but the highest cisco density occurred in waters with a bottom depth around 40 m. We highlight the importance of embayment habitats to cisco restoration and the seasonal migration pattern of cisco identified in this study, which suggests that a restored cisco population can diversify the food web by occupying different habitats from the exotic fishes that now dominate the pelagic waters of Lake Michigan.

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Aquatic food webs that incorporate multiple energy channels (e.g., nearshore benthic and pelagic) with varying productivity and turnover rates convey stability to biological communities by providing independent energy sources. Within the Lake Michigan food web, invasive dreissenid mussels have caused rapid changes to food web structure and potentially altered the channels through which consumers acquire energy. We used stable C and N isotopes to determine how Lake Michigan food web structure has changed in the past decade, coincident with the expansion of dreissenid mussels, decreased pelagic phytoplankton production, and increased nearshore benthic algal production. Fish and invertebrate samples collected from sites around Lake Michigan were analyzed to determine taxa-specific 13C:12C (delta13C) and 15N:14N (delta15N) ratios. Sampling took place during two distinct periods, 2002-2003 and 2010-2012, that spanned the period of dreissenid expansion, and included nearshore, pelagic and profundal fish and invertebrate taxa. The magnitude and direction of the delta13C shift indicated significantly greater reliance upon nearshore benthic energy sources among nearly all fish taxa as well as profundal invertebrates following dreissenid expansion. Although the mechanisms underlying this delta13C shift likely varied among species, possible causes include the transport of benthic algal production to offshore waters and increased feeding on nearshore prey items by pelagic and profundal species. delta15N shifts were more variable and of smaller magnitude across taxa, although declines in delta15N among some pelagic fishes suggest a shift to alternative prey resources. Lake Michigan fishes and invertebrates appear to have responded to dreissenid-induced changes in nutrient and energy pathways by switching from pelagic to alternative nearshore energy subsidies. Although large shifts in energy allocation (i.e., pelagic to nearshore benthic) resulting from invasive species appear to affect total production at upper trophic levels, changes in trophic structure and utilization of novel energy pathways may help to stabilize food webs following species invasions.

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Although islet transplantation may restore insulin independence to individuals with type 1 diabetes mellitus, most have abnormal glucose tolerance. We asked whether the defective glucose tolerance is due to inadequate ß-cell mass or to impaired insulin sensitivity. We performed metabolic studies on four cynomolgus primates before inducing diabetes with streptozotocin (STZ), then again 2-3 weeks after restoring insulin independence via intrahepatic islet transplantation utilizing a calcineurin inhibitor-free immunosuppressive regimen (induction with rabbit antithymocyte globulin and maintenance therapy with rapamycin). Engrafted ß-cell mass was assessed by acute insulin and C-peptide responses to glucose (AIR(glu) and ACR(glu)) and arginine (AIR(arg) and ACR(arg)). Insulin sensitivity (S(I)) was determined in naive and transplanted primates from an intravenous glucose tolerance test using the minimal model. α-Cell function was determined by the acute glucagon response to arginine (AGR(arg)). Glucose tolerance (K(g)) decreased from 4.1 ± 0.5%/min in naive primates to 1.8 ± 0.3%/min in transplanted primates (p < 0.01). Following transplantation, AIR(glu) was 28.7 ± 13.1 µU/ml compared to 169.9 ± 43.1 µU/ml (p < 0.03) in the naive condition, ACR(glu) was 14.5 ± 6.0 ng/ml compared to 96.5 ± 17.0 ng/ml naive (p < 0.01), AIR(arg) was 29.1 ± 13.1 µU/ml compared to 91.4 ± 28.2 µU/ml naive (p < 0.05), and ACR(arg) was 1.11 ± 0.51 ng/ml compared to 2.79 ± 0.77 ng/ml naive (p < 0.05). S(I) did not differ from naive to posttransplant states. AGR(arg) was reduced in transplanted primates (349 ± 118 pg/ml) when compared to both naive (827 ± 354 pg/ml) and post-STZ diabetic primates (1020 ± 440 pg/ml) (p < 0.01 for both comparisons). These data suggest that impaired glucose tolerance observed in islet transplant recipients is secondary to low functional ß-cell mass and not to insulin resistance shortly after transplant. Furthermore, improved glycemic control achieved via islet transplantation over the diabetic state might be attained, in part, via reduced glucagon secretion.

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Climate and dispersal are the two most commonly cited mechanisms to explain spatial synchrony among time series of animal populations, and climate is typically most important for fishes. Using data from 1978-2006, we quantified the spatial synchrony in recruitment and population catch-per-unit-effort (CPUE) for bloater (Coregonus hoyi) populations across lakes Superior, Michigan, and Huron. In this natural field experiment, climate was highly synchronous across lakes but the likelihood of dispersal between lakes differed. When data from all lakes were pooled, modified correlograms revealed spatial synchrony to occur up to 800 km for long-term (data not detrended) trends and up to 600 km for short-term (data detrended by the annual rate of change) trends. This large spatial synchrony more than doubles the scale previously observed in freshwater fish populations, and exceeds the scale found in most marine or estuarine populations. When analyzing the data separately for within- and between-lake pairs, spatial synchrony was always observed within lakes, up to 400 or 600 km. Conversely, between-lake synchrony did not occur among short-term trends, and for long-term trends, the scale of synchrony was highly variable. For recruit CPUE, synchrony occurred up to 600 km between both lakes Michigan and Huron (where dispersal was most likely) and lakes Michigan and Superior (where dispersal was least likely), but failed to occur between lakes Huron and Superior (where dispersal likelihood was intermediate). When considering the scale of putative bloater dispersal and genetic information from previous studies, we concluded that dispersal was likely underlying within-lake synchrony but climate was more likely underlying between-lake synchrony. The broad scale of synchrony in Great Lakes bloater populations increases their probability of extirpation, a timely message for fishery managers given current low levels of bloater abundance.

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PURPOSE: To develop and assess a technique for induction of C peptide-negative diabetes in adult nonhuman primates in preparation for preclinical investigation of type 1 diabetes treatments. MATERIALS AND METHODS: First, temporary embolization of the hepatic and gastric arteries was performed in 14 adult nonhuman primates (six cynomolgus, five rhesus, and three pigtail macaques). After embolization was confirmed with angiography, streptozotocin was injected at a dose of 50-70 mg/kg into the celiac artery and branches supplying the pancreas. The macaques then were given intravenous injections of arginine and glucose, and blood levels of insulin and C peptide were measured with an enzyme-linked immunosorbent assay to determine whether diabetes had been induced. RESULTS: All but one of the macaques developed persistent long-term C peptide-negative diabetes after the streptozotocin injection. One macaque did not develop diabetes after the initial injection and was given a second dose of streoptozotocin, which did induce diabetes. None of the macaques showed any symptoms of hepatic or renal injury, and only one died (of gastric dilatation 5 days after the procedure). CONCLUSION: Streptozotocin injection after temporary embolization of the hepatic and gastric arteries is a safe and reproducible method for inducing C peptide-negative diabetes in adult nonhuman primates in preparation for preclinical investigation of type 1 diabetes treatments.

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BACKGROUND: We reported that rabbit anti-thymocyte globulin (RATG) induction followed by maintenance immunosuppression with sirolimus supports human kidney allograft survival and asked if this combination would promote islet allograft survival in our primate model. METHODS: Using intra-arterial streptozotocin infusion, we rendered four cynomolgus primates diabetic with undetectable C-peptide levels. Animals were maintained on insulin therapy for at least 1 month, and then islets from mixed lymphocyte reaction mismatched primates were infused into the portal vein. Immediately before the islet allotransplant and for 6 additional days, primates were infused with RATG (20 mg/kg) and given a sirolimus dose to achieve a 24-hr trough level of 8 to 14 ng/mL. RESULTS: The regimen resulted in profound peripheral and lymph node lymphocyte depletion for up to 1 month. Repopulation was gradual thereafter. One primate remained insulin-independent for 169 days and rejected after a sirolimus-dose reduction. Two primates died on day 23 while insulin independent because of wound dehiscence, and a third died on day 30 with high sirolimus levels. Liver sections revealed well-vascularized islets with no signs of inflammation. CONCLUSION: Using a nonhuman primate islet transplant model, RATG plus sirolimus supports islet survival as long as proper sirolimus levels are maintained, but the therapy is limited by sirolimus toxicity. Our findings suggest that RATG is not toxic for islets and thus may be considered in future clinical trails while recognizing that sirolimus monotherapy, with its difficult-to-achieve therapeutic dosing, may not be sufficient to maintain long-term islet allograft function in an autoimmune environment.

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