Food web restructuring across an urban estuarine gradient.

Food webs in urban estuaries support valuable ecosystem services that are subject to a wide range of stressors that can degrade the structure of trophic networks. Multiple trophic pathways stabilize food webs by providing complementary diet resources for consumers but the consequences of urbanization on estuarine food webs are relatively unknown. In estuarine creeks across an urban-to-suburban gradient, we demonstrate trophic decoupling of benthic and pelagic pathways, trophic niche contraction, and increasing human health risk arising with the same factors that are associated with ecological degradation. This suggests an urban estuarine paradox-human activities often create larger volumes of deep water habitat, yet human activities also render much of this area unproductive with measurable opportunity costs to food webs. Our findings emphasize the shared consequences of environmental degradation for the ecological integrity of urban estuaries and the health of urban communities that rely on estuaries for sustenance.

Female Pacific walruses (Odobenus rosmarus divergens) show greater partitioning of sea ice organic carbon than males: Evidence from ice algae trophic markers.

The expected reduction of ice algae with declining sea ice may prove to be detrimental to the Pacific Arctic ecosystem. Benthic organisms that rely on sea ice organic carbon (iPOC) sustain benthic predators such as the Pacific walrus (Odobenus rosmarus divergens). The ability to track the trophic transfer of iPOC is critical to understanding its value in the food web, but prior methods have lacked the required source specificity. We analyzed the H-Print index, based on biomarkers of ice algae versus phytoplankton contributions to organic carbon in marine predators, in Pacific walrus livers collected in 2012, 2014 and 2016 from the Northern Bering Sea (NBS) and Chukchi Sea. We paired these measurements with stable nitrogen isotopes (δ15N) to estimate trophic position. We observed differences in the contribution of iPOC in Pacific walrus diet between regions, sexes, and age classes. Specifically, the contribution of iPOC to the diet of Pacific walruses was higher in the Chukchi Sea (52%) compared to the NBS (30%). This regional difference is consistent with longer annual sea ice persistence in the Chukchi Sea. Within the NBS, the contribution of iPOC to walrus spring diet was higher in females (~45%) compared to males (~30%) for each year (p < 0.001), likely due to specific foraging behavior of females to support energetic demands associated with pregnancy and lactation. Within the Chukchi Sea, the iPOC contribution was similar between males and females, yet higher in juveniles than in adults. Despite differences in the origin of organic carbon fueling the system (sea ice versus pelagic derived carbon), the trophic position of adult female Pacific walruses was similar between the NBS and Chukchi Sea (3.2 and 3.5, respectively), supporting similar diets (i.e. clams). Given the higher quality of organic carbon from ice algae, the retreat of seasonal sea ice in recent decades may create an additional vulnerability for female and juvenile Pacific walruses and should be considered in management of the species.

Effects of constant and fluctuating incubation temperatures on hatching success and hatchling traits in the diamondback terrapin (Malaclemys terrapin) in the context of the warming climate.

As global temperatures continue to rise, so too will the nest temperatures of many species of turtles. Yet for most turtle species, including the estuarine diamondback terrapin (Malaclemys terrapin), there is limited information on embryonic sensitivity to elevated temperature. We incubated eggs of M. terrapin at three, mean temperatures (31, 34, 37 °C) under two thermal exposure regimes (constant or semi-naturally fluctuating temperature) and measured hatching success, developmental rate, and hatchling size. Hatching success was 100% at 31 °C and 67% at 34 °C, respectively; at 37 °C, all eggs failed early in the incubation period. These values were unaffected by exposure regime. The modeled LT50 (temperature that was lethal to 50% of the test population) was 34.0 °C in the constant and 34.2 °C in the fluctuating thermal regime, reflecting a steep decline in survival between 33 and 35 °C. Hatchlings having been incubated at a constant 34 °C hatched sooner than those incubated at 31 °C under either constant or fluctuating temperature. Hatchlings were smaller in straight carapace length (CL) and width after having been incubated at 34 °C compared to 31 °C. Larger (CL) hatchlings resulted from fluctuating temperature conditions relative to constant temperature conditions, regardless of mean temperature. Based upon recent temperatures in natural nests, the M. terrapin population studied here appears to possess resiliency to several degrees of elevated mean nest temperatures, beyond which, embryonic mortality will likely sharply increase. When considered within the mosaic of challenges that Maryland's M. terrapin face as the climate warms, including ongoing habitat losses due to sea level rise and impending thermal impacts on bioenergetics and offspring sex ratios, a future increase in embryonic mortality could be a critical factor for a population already experiencing ecological and physiological challenges due to climate change.

Delayed timing of successful spawning of an estuarine dependent fish, black bream Acanthopagrus butcheri.

In this paper, we investigate the period of successful spawning for black bream Acanthopagrus butcheri, an obligate estuarine species in southern Australia that typically spawn in spring and early summer. However, back-calculated spawning dates of juveniles sampled in Gippsland Lakes, Victoria from February to May 2016 indicated that spawning was concentrated over a short period in the Austral mid-summer (January), with a second spawning in late summer and early autumn (late February-early March). Ichthyoplankton sampling in the tributary estuaries from October to early December collected substantial numbers of fish larvae, dominated by gobiids, eleotrids and retropinnids of freshwater origin, but no A. butcheri. The lack of A. butcheri larvae was consistent with the delayed successful spawning indicated by juvenile otolith data. Freshwater flows declined from late winter to summer, with consistent salinity stratification of the water column. Dissolved oxygen (DO) concentrations were generally very low below the halocline. These conditions may have delayed the upstream spawning migration of adults or may have been unsuitable for survival of eggs and newly-hatched larvae. Longer-term predictions for climate change in southern Victoria, including the Gippsland Lakes region, are for lower winter-spring freshwater flows, potentially benefiting the reproductive success of A. butcheri through high water-column stratification, but only if DO concentrations are not compromised by a lack of high winter flows needed to flush low DO water from the system.

Catchment land use predicts benthic vegetation in small estuaries.

Many estuaries are becoming increasingly eutrophic from human activities within their catchments. Nutrient loads often are used to assess risk of eutrophication to estuaries, but such data are expensive and time consuming to obtain. We compared the percent of fertilized land within a catchment, dissolved inorganic nitrogen loads, catchment to estuary area ratio and flushing time as predictors of the proportion of macroalgae to total vegetation within 14 estuaries in south-eastern Australia. The percent of fertilized land within the catchment was the best predictor of the proportion of macroalgae within the estuaries studied. There was a transition to a dominance of macroalgae once the proportion of fertilized land in the catchment exceeded 24%, highlighting the sensitivity of estuaries to catchment land use.

Metabolic rates are elevated and influenced by maternal identity during the early, yolk-dependent, post-hatching period in an estuarine turtle, the diamondback terrapin (Malaclemys terrapin).

Non-genetic maternal effects, operating through a female's physiology or behavior, can influence offspring traits and performance. Here we examined potential maternal influences on metabolic rates (MR) of offspring in an estuarine turtle, the diamondback terrapin (Malaclemys terrapin). Females and their eggs were collected from the field and the eggs incubated in the laboratory for subsequent measurement of MR of females, late-stage embryos, newly-hatched individuals that were nutritionally dependent on yolk, and older hatchlings that had depleted their yolk reserves and thus were independent of energetic contributions from the female. Female identity significantly affected MR of yolk-dependent hatchlings but, after yolk was depleted, MR of offspring converged and no longer reflected the maternal influence. Offspring from different females also differed in size, which influenced offspring MR and growth, but there was no correlation between female MR or size and offspring traits. MR of the older, yolk-independent hatchlings was lower overall than yolk-dependent hatchlings but correlated positively with growth rates and prior developmental rate (e.g. negatively correlated with time to hatching). Unlike another turtle species (snapping turtles), in which maternally-related differences in offspring MR were retained after yolk depletion, the maternal influence on offspring MR in diamondback terrapins is limited to early hatchling development and growth. The transient nature of the maternal effect, which was present only during the period that hatchlings were metabolizing yolk, suggests that variation among females in the composition of yolk deposited in eggs could be responsible for the differences observed in this study.

Using stable isotope ratios to estimate atmospheric nitrogen fixed by cyanobacteria at the ecosystem scale.

Diazotrophic cyanobacteria are capable of fixing atmospheric N2 to satisfy their physiological nitrogen requirements. This process can result in the transfer of substantial amounts of "new" diazotrophic nitrogen (ND) to aquatic ecosystems during blooms of these taxa. Using in situ measurements of plankton natural abundance stable isotope composition and a combination of underway and fixed site survey data, the total N(D) flux into the Gippsland Lakes estuary (Australia) was estimated during a summer bloom of the diazotrophic cyanobacterium Nodularia spumigena. Over the course of the bloom, N(D) increased in the upper water column of the estuary from 33% +/- 17% (mean +/- SD) to 73% +/- 13% of the standing pool of total particulate N. A conservative estimate of total N(D) flux (146 Mg) equates to an estimated 177% of the summer total N load and 22% of the annual total N load to the estuary. Combining natural abundance stable isotope measurements with relatively simple fixed and underway survey designs can provide a cost-effective approach for monitoring the N(D) flux into estuary or lacustrine environments. This approach relies on an isotopic differential between the diazotrophic and the non-diazotrophic components of the plankton community; it may not be appropriate in ecosystems that experience low-level blooms or blooms of intermittent N-fixing cyanobacteria. Large-scale blooms of diazotrophic cyanobacteria are considered uncommon in estuaries, yet it is clear that these blooms can represent major sources of new N to estuarine ecosystems when and where they occur.

Assimilation of diazotrophic nitrogen into pelagic food webs.

The fate of diazotrophic nitrogen (N(D)) fixed by planktonic cyanobacteria in pelagic food webs remains unresolved, particularly for toxic cyanophytes that are selectively avoided by most herbivorous zooplankton. Current theory suggests that N(D) fixed during cyanobacterial blooms can enter planktonic food webs contemporaneously with peak bloom biomass via direct grazing of zooplankton on cyanobacteria or via the uptake of bioavailable N(D) (exuded from viable cyanobacterial cells) by palatable phytoplankton or microbial consortia. Alternatively, N(D) can enter planktonic food webs post-bloom following the remineralization of bloom detritus. Although the relative contribution of these processes to planktonic nutrient cycles is unknown, we hypothesized that assimilation of bioavailable N(D) (e.g., nitrate, ammonium) by palatable phytoplankton and subsequent grazing by zooplankton (either during or after the cyanobacterial bloom) would be the primary pathway by which N(D) was incorporated into the planktonic food web. Instead, in situ stable isotope measurements and grazing experiments clearly documented that the assimilation of N(D) by zooplankton outpaced assimilation by palatable phytoplankton during a bloom of toxic Nodularia spumigena Mertens. We identified two distinct temporal phases in the trophic transfer of N(D) from N. spumigena to the plankton community. The first phase was a highly dynamic transfer of N(D) to zooplankton with rates that covaried with bloom biomass while bypassing other phytoplankton taxa; a trophic transfer that we infer was routed through bloom-associated bacteria. The second phase was a slowly accelerating assimilation of the dissolved-N(D) pool by phytoplankton that was decoupled from contemporaneous variability in N. spumigena concentrations. These findings provide empirical evidence that N(D) can be assimilated and transferred rapidly throughout natural plankton communities and yield insights into the specific processes underlying the propagation of N(D) through pelagic food webs.

Incorporating temporally dynamic baselines in isotopic mixing models.

Stable isotopes (particularly C and N) are widely used to make inferences regarding food web structure and the phenology of consumer diet shifts, applications that require accurate isotopic characterization of trophic resources to avoid biased inferences of feeding relationships. For example, most isotope mixing models require that endmembers be adequately represented by a single probability distribution; yet, there is mounting evidence that the isotopic composition of aquatic organisms often used as mixing model endmembers can change over periods of weeks to months. A review of the literature indicated that the delta13C values of five aquatic primary consumer taxa, commonly used as proxies of carbon production sources (i.e., trophic baselines), express seasonally dynamic cycles characterized by an oscillation between summer maxima and winter minima. Based on these results, we built a dynamic baseline mixing model that allows a growing consumer to track temporal gradients in the isotopic baselines of a food web. Simulations showed that the ability of a consumer to maintain or approach isotopic equilibrium with its diet over a realistic growth season was strongly affected by both the rate of change of the isotopic baseline and equilibration rate of the consumer. In an empirical application, mixing models of varying complexity were used to estimate the relative contribution of benthic vs. pelagic carbon sources to nine species of juvenile fish in a fluvial lake of the St. Lawrence River system (Québec, Canada). Estimates of p (proportion of carbon derived from benthic sources) derived from a static mixing model indicated broad interspecific variation in trophic niche, ranging from complete benthivory to > 95% reliance on pelagic food webs. Output from the more realistic dynamic baseline mixing model increased estimated benthivory by an average of 36% among species. Taken together, our results demonstrate that failing to identify dynamic baselines when present, and (or) matching consumers with baseline taxa that possess substantially different equilibration rates can seriously bias interpretation of stable isotope data. Additionally, by providing a formalized framework that allows both resources and consumers to shift their isotopic value through time, our model demonstrates a feasible approach for incorporating temporally dynamic isotope conditions in trophic studies of higher consumers.

Variability and directionality of temporal changes in δ(13)C and δ (15)N of aquatic invertebrate primary consumers.

Seasonal oscillations in the carbon (δ(13)C) and nitrogen (δ(15)N) isotope signatures of aquatic algae can cause seasonal enrichment-depletion cycles in the isotopic composition of planktonic invertebrates (e.g., copepods). Yet, there is growing evidence that seasonal enrichment-depletion cycles also occur in the isotope signatures of larger invertebrate consumers, taxa used to define reference points in isotope-based trophic models (e.g., trophic baselines). To evaluate the general assumption of temporal stability in non-zooplankton aquatic invertebrates, δ(13)C and δ(15)N time series data from the literature were analyzed for seasonality and the influence of biotic (feeding group) and abiotic (trophic state, climate regime) factors on isotope temporal patterns. The amplitude of δ(13)C and δ(15)N enrichment-depletion cycles was negatively related to body size, although all size-classes of invertebrates displayed a winter-to-summer enrichment in δ(13)C and depletion in δ(15)N. Among feeding groups, periphytic grazers were more variable and displayed larger temporal changes in δ(13)C than detritivores. For nitrogen, temporal variability and magnitude of directional change of δ(15)N was most strongly related to ecosystem trophic state (eutrophic > mesotrophic, oligotrophic). This study provides evidence of seasonality in the isotopic composition of aquatic invertebrates across very broad geographical and ecological gradients as well as identifying factors that are likely to modulate the strength and variability of seasonality. These results emphasize the need for researchers to recognize the likelihood of temporal changes in non-zooplankton aquatic invertebrate consumers at time scales relevant to seasonal studies and, if present, to account for temporal dynamics in isotope trophic models.