Food Web Assembly at the Landscape Scale: Using Stable Isotopes to Reveal Changes in Trophic Structure During Succession

Food webs are increasingly evaluated at the landscape scale, accounting for spatial interactions involving different nutrient and energy channels. Also, while long viewed as static, food webs are increasingly seen as dynamic entities that assemble during vegetation succession. The next necessary step is, therefore, to link nutrient flows between ecosystems to local food web assembly processes. In this study, we used a 100-year salt marsh succession in which we investigated the long-term changes in food web organization, especially focusing on the balance between internal versus external nutrient sources. We found that during food web assembly, the importance of internal (terrestrial) nutrient cycling increases at the expense of external (marine) inputs. This change from external to internal nutrient cycling is associated with strong shifts in the basis of energy channels within the food web. In early succession, detritivores are mostly fuelled by marine inputs whereas in later succession they thrive on locally produced plant litter, with consequences for their carnivores. We conclude that this 100 years of food web assembly proceeds by gradual decoupling of terrestrial nutrient cycling from the marine environment, and by associated rearrangements in the herbivore and detritivore energy channels. Food web assembly thus interacts with nutrient and energy flows across ecosystem boundaries.     

Source Partitioning Using Stable Isotopes: Coping with Too Much Variation

Background

Stable isotope analysis is increasingly being utilised across broad areas of ecology and biology. Key to much of this work is the use of mixing models to estimate the proportion of sources contributing to a mixture such as in diet estimation.

Methodology

By accurately reflecting natural variation and uncertainty to generate robust probability estimates of source proportions, the application of Bayesian methods to stable isotope mixing models promises to enable researchers to address an array of new questions, and approach current questions with greater insight and honesty.

Conclusions

We outline a framework that builds on recently published Bayesian isotopic mixing models and present a new open source R package, SIAR. The formulation in R will allow for continued and rapid development of this core model into an all-encompassing single analysis suite for stable isotope research.     

Using Stable Isotopes to Differentiate Trophic Feeding Channels within Soil Food Webs

The soil is probably the most diverse habitat there is, with organisms ranging in sizes from less than 1 μm to several metres in length. However, it is increasingly evident that we know little about the interactions occurring between these organisms, the functions that they perform as individual species, or together within their different feeding guilds. These interactions between groups of organisms and physical and chemical processes shape the soil as a habitat and influence the nature of the soil food web with consequences for the above‐ground vegetation and food web. Protists are known as one of the most abundant groups of bacterivores within the soil; however, they are also consumers of a number of other food sources. Even though they are responsible for a large proportion of the mineralisation of bacterial biomass and have a large impact on the C and N cycles within the soil they are regularly overlooked when investigating the complete soil food web. Recently, stable isotopes have been used to determine trophic interactions and here we describe how this technique has been used to highlight linkages between protists and the soil food web.     

Stable Isotopes in Fish Eye Lenses as Potential Recorders of Trophic and Geographic History

We evaluated eye lenses as potential recorders of stable isotope histories in fish because they consist of metabolically inert optical proteins that are deposited in successive, concentric circles (laminae) much like otolith circuli and tree rings. We conducted four different tests on lenses from red snapper, red grouper, gag, and white grunt. The first test was a low-resolution screening of multiple individuals (4–5 radial groups of laminae per lens, all species except white grunt). Along the radial axis, all individuals exhibited substantial isotopic variability. Red snapper individuals separated into two groups based on δ ¹⁵N and gag separated into two groups based on δ ¹³C. Two gag with the greatest variation were chosen for high-resolution temporal analysis using individual laminae from their second eye lenses. The first-order patterns from the high-resolution analysis generally mimicked patterns from the low-resolution screening of grouped laminae, yet the high-resolution plots revealed early-life details that were not apparent in the low-resolution screenings. For the third test, left- versus right-eye variation was compared using high-resolution methods. White grunt left- and right-eye radial isotopic patterns were almost identical for both δ ¹³C and δ ¹⁵N, suggesting the variations observed among individual fish were not artifacts. The final test evaluated intra-laminar variation; multiple samples were analyzed from different parts of the same lamina. Seven laminae from three individuals of two species were analyzed in this manner; variations among laminae were found to be much higher than variations within laminae. However, nominal intra-laminar variations were comparable to nominal differences between left and right lenses, suggesting intra-laminar variation established measurement precision. Eye lens isotopes appear to be useful for reconstructing the isotopic histories of individual fish; these histories can be compared with spatially-derived isoscapes to reconstruct individual histories for site fidelity, movement and trophic position.     

用稳定性同位素技术确定高寒草甸生态系统中动物营养级模型

根据稳定性同位素技术原理建立了高寒草甸生态系统中动物的营养级模型 (3)、 (7)和 (9)式。 3个模型分别描述了每种食物资源对动物的贡献大小 (PCV)、食物资源 (Ai)占取食动物 (P)的整个食物的比例 (PAiP)、动物在高寒草甸生态系统中的营养级 (TLc) :PCVAi =cos (ΔαPAi)ΖPAi(3)PAiP =PCVAi∑i=1PCVAi× % (7)TLc =1 (αc-αTL1) /Δαcd (9)式中 ,ΔαPAi为捕食者P与食物Ai 的取食角 ,ΖPAi为捕食向量与食物向量之间的欧氏距离 ,αc 是消费者的向量角 ,αTL1是第一营级的向量角 ,利用系数Δαcd是消费者与食物向量角之差 (为一常数 )。同时 ,给出了判断高寒草甸两个物种之间捕食或营养关系模型 (ΖS1 S2 ) :当cos (Δα) /PCVmin≤ΖS1 S2 ≤cos (Δα) /PCVmax时存在捕食关系 ,并为上下级营养关系 ;当ΖS1 S2 cos (Δα) /PCVmax时 ,不存在捕食关系 ,前式为同一营养级 ,后式为相隔一个至几个营养级。模型 (9)式得到的结果与张晓爱等 (1999)报道一致。     

Trophic Discrimination Factors of Stable Carbon and Nitrogen Isotopes in Hair of Corn Fed Wild Boar

Stable isotope measurements are increasingly being used to gain insights into the nutritional ecology of many wildlife species and their role in ecosystem structure and function. Such studies require estimations of trophic discrimination factors (i.e. differences in the isotopic ratio between the consumer and its diet). Although trophic discrimination factors are tissue- and species- specific, researchers often rely on generalized, and fixed trophic discrimination factors that have not been experimentally derived. In this experimental study, captive wild boar (Sus scrofa) were fed a controlled diet of corn (Zea mays), a popular and increasingly dominant food source for wild boar in the Czech Republic and elsewhere in Europe, and trophic discrimination factors for stable carbon (Δ¹³C) and nitrogen (Δ¹⁵N) isotopes were determined from hair samples. The mean Δ¹³C and Δ¹⁵N in wild boar hair were –2.3 ‰ and +3.5 ‰, respectively. Also, in order to facilitate future derivations of isotopic measurements along wild boar hair, we calculated the average hair growth rate to be 1.1 mm d^-1. Our results serve as a baseline for interpreting isotopic patterns of free-ranging wild boar in current European agricultural landscapes. However, future research is needed in order to provide a broader understanding of the processes underlying the variation in trophic discrimination factors of carbon and nitrogen across of variety of diet types.     

Trophic Strategies of a Non-Native and a Native Amphibian Species in Shared Ponds

One of the critical factors for understanding the establishment, success and potential impact on native species of an introduced species is a thorough knowledge of how these species manage trophic resources. Two main trophic strategies for resource acquisition have been described: competition and opportunism. In the present study our objective was to identify the main trophic strategies of the non-native amphibian Discoglossus pictus and its potential trophic impact on the native amphibian Bufo calamita. We determine whether D. pictus exploits similar trophic resources to those exploited by the native B. calamita (competition hypothesis) or alternative resources (opportunistic hypothesis). To this end, we analyzed the stable isotope values of nitrogen and carbon in larvae of both species, in natural ponds and in controlled laboratory conditions. The similarity of the δ¹⁵N and δ¹³C values in the two species coupled with isotopic signal variation according to pond conditions and niche partitioning when they co-occurred indicated dietary competition. Additionally, the non-native species was located at higher levels of trophic niches than the native species and B. calamita suffered an increase in its standard ellipse area when it shared ponds with D. pictus. These results suggest niche displacement of B. calamita to non-preferred resources and greater competitive capacity of D. pictus in field conditions. Moreover, D. pictus showed a broader niche than the native species in all conditions, indicating increased capacity to exploit the diversity of resources; this may indirectly favor its invasiveness. Despite the limitations of this study (derived from potential variability in pond isotopic signals), the results support previous experimental studies. All the studies indicate that D. pictus competes with B. calamita for trophic resources with potential negative effects on the fitness of the latter.     

Dietary Plasticity of Generalist and Specialist Ungulates in the Namibian Desert: A Stable Isotopes Approach

Desert ungulates live in adverse ecosystems that are particularly sensitive to degradation and global climate change. Here, we asked how two ungulate species with contrasting feeding habits, grazing gemsbok (Oryx g. gazella) and browsing springbok (Antidorcas marsupialis), respond to an increase in food availability during a pronounced rain period. We used a stable isotope approach to delineate the feeding habits of these two ungulates in the arid Kunene Region of Namibia. Our nineteen months field investigation included two time periods of drought when food availability for ungulates was lowest and an intermediate period with extreme, unusual rainfalls. We documented thirteen isotopically distinct food sources in the isotopic space of the study area. Our results indicated a relatively high dietary plasticity of gemsbok, which fed on a mixture of plants, including more than 30% of C3 plants during drought periods, but almost exclusively on C4 and CAM plant types when food was plentiful. During drought periods, the inferred gemsbok diets also consisted of up to 25% of Euphorbia damarana; an endemic CAM plant that is rich in toxic secondary plant compounds. In contrast, springbok were generalists, feeding on a higher proportion of C3 than C4/CAM plants, irrespective of environmental conditions. Our results illustrate two dietary strategies in gemsbok and springbok which enable them to survive and coexist in the hostile Kunene arid ecosystem.     

Stable Isotopes and Zooarchaeology at Teotihuacan,Mexico Reveal Earliest Evidence of Wild Carnivore Management in Mesoamerica

From Roman gladiatorial combat to Egyptian animal mummies, the capture and manipulation of carnivores was instrumental in helping to shape social hierarchies throughout the ancient world. This paper investigates the historical inflection point when humans began to control animals not only as alimental resources but as ritual symbols and social actors in the New World. At Teotihuacan (A.D. 1–550), one of the largest pre-Hispanic cities, animal remains were integral components of ritual caches expressing state ideology and militarism during the construction of the Moon and the Sun Pyramids. The caches contain the remains of nearly 200 carnivorous animals, human sacrificial victims and other symbolic artifacts. This paper argues the presence of skeletal pathologies of infectious disease and injuries manifest on the carnivore remains show direct evidence of captivity. Stable isotope analysis (δ¹³C and δ¹⁵N) of bones and teeth confirms that some of these carnivores were consuming high levels of C₄ foods, likely reflecting a maize-based anthropocentric food chain. These results push back the antiquity of keeping captive carnivores for ritualistic purposes nearly 1000 years before the Spanish conquistadors described Moctezuma’s zoo at the Aztec capital. Mirroring these documents the results indicate a select group of carnivores at Teotihuacan may have been fed maize-eating omnivores, such as dogs and humans. Unlike historical records, the present study provides the earliest and direct archaeological evidence for this practice in Mesoamerica. It also represents the first systematic isotopic exploration of a population of archaeological eagles (n = 24) and felids (n = 29).     

Stable Isotopes Reveal Long-Term Fidelity to Foraging Grounds in the Galapagos Sea Lion (Zalophus wollebaeki)

Most otariids have colony-specific foraging areas during the breeding season, when they behave as central place foragers. However, they may disperse over broad areas after the breeding season and individuals from different colonies may share foraging grounds at that time. Here, stable isotope ratios in the skull bone of adult Galapagos sea lions (Zalophus wollebaeki) were used to assess the long-term fidelity of both sexes to foraging grounds across the different regions of the Galapagos archipelago. Results indicated that the stable isotope ratios (δ¹³C and δ¹⁵N) of sea lion bone significantly differed among regions of the archipelago, without any significant difference between sexes and with a non significant interaction between sex and region. Moreover, standard ellipses, estimated by Bayesian inference and used as a measure of the isotopic resource use area at the population level, overlapped widely for the sea lions from the southern and central regions, whereas the overlap of the ellipses for sea lions from the central and western regions was small and non-existing for those from the western and southern regions. These results suggest that males and females from the same region within the archipelago use similar foraging grounds and have similar diets. Furthermore, they indicate that the exchange of adults between regions is limited, thus revealing a certain degree of foraging philopatry at a regional scale within the archipelago. The constraints imposed on males by an expanded reproductive season (~ 6 months), resulting from the weak reproductive synchrony among females, and those imposed on females by a very long lactation period (at least one year but up to three years), may explain the limited mobility of adult Galapagos sea lions of both sexes across the archipelago.     

Invasive Mussels Alter the Littoral Food Web of a Large Lake: Stable Isotopes Reveal Drastic Shifts in Sources and Flow of Energy

We investigated how establishment of invasive dreissenid mussels impacted the structure and energy sources of the littoral benthic food web of a large temperate lake. We combined information about pre- and postdreissenid abundance, biomass, and secondary production of the littoral benthos with results of carbon and nitrogen stable isotope analysis of archival (predreissenid) and recent (postdreissenid) samples of all common benthic taxa. This approach enabled us to determine the importance of benthic and sestonic carbon to the littoral food web before, and more than a decade after dreissenid establishment. Long term dreissenid presence was associated with a 32-fold increase in abundance, 6-fold increase in biomass, and 14-fold increase in secondary production of the littoral benthos. Dreissenids comprised a large portion of the post-invasion benthos, making up 13, 38, and 56% of total abundance, biomass, and secondary production, respectively. The predreissenid food web was supported primarily by benthic primary production, while sestonic material was relatively more important to the postdreissenid food web. The absolute importance of both sestonic material and benthic primary production to the littoral benthos increased considerably following dreissenid establishment. Our results show drastic alterations to food web structure and suggest that dreissenid mussels redirect energy and material from the water column to the littoral benthos both through biodeposition of sestonic material as well as stimulation of benthic primary production.     

Tree-Ring Stable Isotopes Reveal Twentieth-Century Increases in Water-Use Efficiency of Fagus sylvatica and Nothofagus spp. in Italian and Chilean Mountains

Changes in intrinsic water use efficiency (iWUE) were investigated in Fagus sylvatica and Nothofagus spp. over the last century. We combined dendrochronological methods with dual-isotope analysis to investigate whether atmospheric changes enhanced iWUE of Fagus and Nothofagus and tree growth (basal area increment, BAI) along latitudinal gradients in Italy and Chile. Post-maturation phases of the trees presented different patterns in δ¹³C, Δ¹³C, δ¹⁸O, Ci (internal CO₂ concentration), iWUE, and BAI. A continuous enhancement in isotope-derived iWUE was observed throughout the twentieth century, which was common to all sites and related to changes in Ca (ambient CO₂ concentration) and secondarily to increases in temperature. In contrast to other studies, we observed a general increasing trend of BAI, with the exception of F. sylvatica in Aspromonte. Both iWUE and BAI were uncoupled with the estimated drought index, which is in agreement with the absence of enduring decline in tree growth. In general, δ¹³C and δ¹⁸O showed a weak relationship, suggesting the major influence of photosynthetic rate on Ci and δ¹³C, and the minor contribution of the regulation of stomatal conductance to iWUE. The substantial warming observed during the twentieth century did not result in a clear pattern of increased drought stress along these latitudinal transects, because of the variability in temporal trends of precipitation and in specific responses of populations.     

Larval Environment Alters Amphibian Immune Defenses Differentially across Life Stages and Populations

Recent global declines, extirpations and extinctions of wildlife caused by newly emergent diseases highlight the need to improve our knowledge of common environmental factors that affect the strength of immune defense traits. To achieve this goal, we examined the influence of acidification and shading of the larval environment on amphibian skin-associated innate immune defense traits, pre and post-metamorphosis, across two populations of American Bullfrogs (Rana catesbeiana), a species known for its wide-ranging environmental tolerance and introduced global distribution. We assessed treatment effects on 1) skin-associated microbial communities and 2) post-metamorphic antimicrobial peptide (AMP) production and 3) AMP bioactivity against the fungal pathogen Batrachochytrium dendrobatidis (Bd). While habitat acidification did not affect survival, time to metamorphosis or juvenile mass, we found that a change in average pH from 7 to 6 caused a significant shift in the larval skin microbial community, an effect which disappeared after metamorphosis. Additionally, we found shifts in skin-associated microbial communities across life stages suggesting they are affected by the physiological or ecological changes associated with amphibian metamorphosis. Moreover, we found that post-metamorphic AMP production and bioactivity were significantly affected by the interactions between pH and shade treatments and interactive effects differed across populations. In contrast, there were no significant interactions between treatments on post-metamorphic microbial community structure suggesting that variation in AMPs did not affect microbial community structure within our study. Our findings indicate that commonly encountered variation in the larval environment (i.e. pond pH and degree of shading) can have both immediate and long-term effects on the amphibian innate immune defense traits. Our work suggests that the susceptibility of amphibians to emerging diseases could be related to variability in the larval environment and calls for research into the relative influence of potentially less benign anthropogenic environmental changes on innate immune defense traits.     

Photosynthetic Fractionation of the Stable Isotopes of Oxygen and Carbon

Isotope discrimination during photosynthetic exchange of O2 and CO2 was measured using enzyme, thylakoid, and whole cell preparations. Evolved oxygen from isolated spinach thylakoids was isotopically identical (within analytical error) to its source water. Similar results were obtained with Anacystis nidulans Richter and Phaeodactylum tricornutum Bohlin cultures purged with helium. For consumptive reactions, discrimination ([delta], where 1 + [delta]/1000 equals the isotope effect, k16/k18 or k12/k13) was determined by analysis of residual substrate (O2 or CO2). The [delta] for the Mehler reaction, mediated by ferredoxin or methylviologen, was 15.3[per mille (thousand) sign]. Oxygen isotope discrimination during oxygenation of ribulose-1,5-bisphosphate (RuBP) catalyzed by RuBP carboxylase/oxygenase (Rubisco) was 21.3[per mille (thousand) sign] and independent of enzyme source, unlike carbon isotope discrimination: 30.3[per mille (thousand) sign] for spinach enzyme and 19.6 to 23[per mille (thousand) sign] for Rhodospirillum rubrum and A. nidulans enzymes, depending on reaction conditions. The [delta] for O2 consumption catalyzed by glycolate oxidase was 22.7[per mille (thousand) sign]. The expected overall [delta] for photorespiration is about 21.7[per mille (thousand) sign]. Consistent with this, when Asparagus sprengeri Regel mesophyll cells approached the compensation point within a sealed vessel, the [delta]18O of dissolved O2 came to a steady-state value of about 21.5[per mille (thousand) sign] relative to the source water. The results provide improved estimates of discrimination factors in several reactions prominent in the global O cycle and indicate that photorespiration plays a significant part in determining the isotopic composition of atmospheric oxygen.     

Diets of Introduced Predators Using Stable Isotopes and Stomach Contents

ABSTRACT In a study of predation on ground-nesting birds at South San Francisco Bay (South Bay), California, USA, we analyzed stomach contents and stable isotopes of carbon and nitrogen to identify commonly consumed prey. We obtained the stomach contents from 206 nonnative red foxes (Vulpes vulpes regalis) collected in the South Bay area and Monterey County during 1995–2001 and from 68 feral cats (Felis silvestris) from the South Bay area during 2001–2002. We determined prey identity, biomass, and frequency, described seasonal diet trends, and derived an Index of Relative Importance. Avian species were the most frequent prey we found in the stomachs of red foxes from South Bay (61%), whereas small rodents were most frequent for red foxes from Monterey County (62%). Small rodents were the most frequent prey we found in feral cats (63%). Carbon and nitrogen isotopic signatures for foxes supported stomach content findings. However, isotope results indicated that cats received a majority of their energy from a source other than rodents and outside the natural system, which differed from the stomach content analysis. We demonstrated the utility of both stable isotope and stomach content analyses to establish a more complete understanding of predators' diets. This information aids natural resource managers in planning and evaluating future predator-removal programs and increases our understanding of the impacts of nonnative foxes and cats on native species.     

Feeding Strategies and Trophic Niche Divergence of Three Groups of Dosidicus gigas off Peru: Based on Stable Carbon and Nitrogen Isotopes and Morphology of Feeding Apparatuses

Marine Biotechnology - Dosidicus gigas (D. gigas) is a pelagic cephalopod of ecological and economic importance widely distributed in the eastern Pacific Ocean. Generally, small-, medium-, and...