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Longer and Less Overlapping Food Webs in Anthropogenically Disturbed Marine Ecosystems: Confirmations from the Past

  • Fabiana Saporiti ,

    Affiliation Department of Animal Biology and Institut de Recerca de la Biodiversitat (IRBio), Faculty of Biology, University of Barcelona, Barcelona, Spain

  • Stuart Bearhop,

    Affiliation Centre for Ecology and Conservation, School of Biosciences, University of Exeter, Cornwall Campus, Penryn, United Kingdom

  • Laura Silva,

    Affiliation Laboratory of Marine Mammals, Centro Nacional Patagónico - Consejo Nacional de Investigaciones Científicas y Técnicas (CENPAT-CONICET), Puerto Madryn, Argentina

  • Damián G. Vales,

    Affiliation Laboratory of Marine Mammals, Centro Nacional Patagónico - Consejo Nacional de Investigaciones Científicas y Técnicas (CENPAT-CONICET), Puerto Madryn, Argentina

  • Lisette Zenteno,

    Affiliation Department of Animal Biology and Institut de Recerca de la Biodiversitat (IRBio), Faculty of Biology, University of Barcelona, Barcelona, Spain

  • Enrique A. Crespo,

    Affiliation Laboratory of Marine Mammals, Centro Nacional Patagónico - Consejo Nacional de Investigaciones Científicas y Técnicas (CENPAT-CONICET), Puerto Madryn, Argentina

  • Alex Aguilar,

    Affiliation Department of Animal Biology and Institut de Recerca de la Biodiversitat (IRBio), Faculty of Biology, University of Barcelona, Barcelona, Spain

  • Luis Cardona

    Affiliation Department of Animal Biology and Institut de Recerca de la Biodiversitat (IRBio), Faculty of Biology, University of Barcelona, Barcelona, Spain

Longer and Less Overlapping Food Webs in Anthropogenically Disturbed Marine Ecosystems: Confirmations from the Past

  • Fabiana Saporiti, 
  • Stuart Bearhop, 
  • Laura Silva, 
  • Damián G. Vales, 
  • Lisette Zenteno, 
  • Enrique A. Crespo, 
  • Alex Aguilar, 
  • Luis Cardona


The human exploitation of marine resources is characterised by the preferential removal of the largest species. Although this is expected to modify the structure of food webs, we have a relatively poor understanding of the potential consequences of such alteration. Here, we take advantage of a collection of ancient consumer tissues, using stable isotope analysis and SIBER to assess changes in the structure of coastal marine food webs in the South-western Atlantic through the second half of the Holocene as a result of the sequential exploitation of marine resources by hunter-gatherers, western sealers and modern fishermen. Samples were collected from shell middens and museums. Shells of both modern and archaeological intertidal herbivorous molluscs were used to reconstruct changes in the stable isotopic baseline, while modern and archaeological bones of the South American sea lion Otaria flavescens, South American fur seal Arctocephalus australis and Magellanic penguin Spheniscus magellanicus were used to analyse changes in the structure of the community of top predators. We found that ancient food webs were shorter, more redundant and more overlapping than current ones, both in northern-central Patagonia and southern Patagonia. These surprising results may be best explained by the huge impact of western sealing on pinnipeds during the fur trade period, rather than the impact of fishing on fish populations. As a consequence, the populations of pinnipeds at the end of the sealing period were likely well below the ecosystem's carrying capacity, which resulted in a release of intraspecific competition and a shift towards larger and higher trophic level prey. This in turn led to longer and less overlapping food webs.


Human activities have altered most of the coastal marine ecosystems of the world over many centuries, causing reductions in population sizes, shifts in geographic ranges, and losses of diversity, biomass, and ecosystem functioning [1], [2], [3], [4], [5], [6]. Both aboriginal and industrial exploitation of marine resources are characterised by the preferential removal of the largest species [3], [7], [8], [9], [10], a process thought to shorten size-structured marine food webs [4], [11], [12]. However, so far, megafaunal exploitation has generally resulted in population collapse and top predator rarity, rather than in true extinctions [13], [14], [15]. The difference between rarity and extinction is relevant, because the extinct species no longer belong to the local food web, whereas the scarce ones remain, although it has been argued that these can be considered functionally extinct [10], [16].

To understand the actual relevance of both extinction and scarcity of formerly abundant megafauna species, we need to assess their role in the pristine ecosystems in which they have evolved. This can be achieved by studying marine protected areas (e.g. [17]) but the influence of the human disturbed matrix in which they are embedded is difficult to control. Furthermore, marine reserves are often too small to support viable populations of large top predators or encompass entire foraging ranges [18] and have not been protected for long enough to guarantee full recovery [19]. A second approach is through ecosystem modelling (e.g. [20], [21]), but this can be hampered by the limited perspective of contemporary data [3], the difficulties of model parameterisation [22] and unknown changes in the diet and foraging behaviour of predators through time (e.g. [23], [24]). A third approach consists of using ancient biological material, such as bones and shells, to reconstruct trophic relationships in a time span prior to the anthropogenic alteration of marine ecosystems [3].

The mechanisms and underlying causes of a number of cases of population collapses or extinctions have been clarified by analysing the fossil and zooarchaeological records (e.g. [25]). However, this method brings little information about past diets, trophic levels and food-web structure. The development of stable isotope analyses and quantitative methods for analysing the food-web topology [26], [27], [28] allows the reconstruction of past trophic relationships based on ancient biological material [29], since the stable isotope ratios in consumer tissues represent those of their diet in a predictable manner [30], [31]. The marine ecosystems off Argentina have suffered major anthropogenic changes during the past two centuries. Firstly, European sealers locally extirpated the South American fur seal (Arctocephalus australis) during the 19th century and were at least in part responsible for a decline in South American sea lion populations (Otaria flavescens) during the first half of the 20th century [32], [33], [34], [35], [36]. When exploitation ceased most populations of this species had been reduced to <10% of the pre-exploitation numbers and their recovery did not begin until the early 1990s in Argentina, after several decades of stagnation [34], [37], [38]. As a result, the current populations of both species are still well below pre-exploitation numbers [34], [39], [40], [41], [42]. Furthermore, fisheries targeting large demersal fishes were established in Río de la Plata and northern Patagonia in the 1970s, causing a population decline in several large benthic predatory fish species [43], [44], [45], [46]. Finally, the Argentine population of the Magellanic penguin (Spheniscus magellanicus) increased during the 20th century, both in number of individuals and geographic range [47], perhaps due to the decline of competitors and predators because of the exploitation of pinnipeds [48].

However, the European sealers and fishermen were not the first humans to exploit the marine resources off Argentina. Aboriginal hunter-gatherers began to exploit the local populations of fur seals, sea lions and other marine species during the middle Holocene [49], [50], [51], [52], [53], [54]. Even though the general opinion is that the impact on the populations of pinnipeds was minimal [49], [55]. More recently, Zangrando and colleagues [56] argued that human pressures on fur seals in the Beagle Channel during the late Holocene might have resulted in demographic and ecological changes, based on evidence from stable isotope analyses and the decreasing age and size of hunted individuals. However, these results remain inconclusive because potential variations of the stable isotope baseline through time were not accounted for [57]. The zooarchaeological record preserved in the hunter-gatherers middens offers an excellent opportunity to reconstruct the structure of ancient marine food webs (while accounting for potential changes in stable isotopic baselines) in the South-western Atlantic and compare it with that of modern food webs.

In this paper, we use the stable isotopes of carbon and nitrogen from the shells of mollusc shells to set the stable isotopic baseline and from bones of marine mammals and penguins to reconstruct the changes in the topology of coastal food webs from central-northern Patagonia and southern Patagonia through the second half of the Holocene. Through this, we aim to assess whether the structure of the food web has changed as a consequence of human exploitation during the studied period.

Material and Methods

Ethics Statement

Permits to collect modern samples (Table 1 and S1) were issued by the “Dirección de Fauna y Flora Silvestre”, and the “Dirección de Areas Protegidas”, both from the Province of Chubut. The zooarchaeological samples come from previous fieldwork carried out by Julieta Gómez Otero, Florencia Borrella, Martín Serrán and Lorena Peralta in Golfo San Matías and Península Valdés (central-northern Patagonia), Eduardo Moreno in Santa Cruz (southern Patagonia) and Ernesto Piana, Luis Orquera, Angie Tivoli and Francisco Zangrando in the Beagle Channel (Tierra del Fuego). All the samples used for this study come from stranded animals, died naturally (except for mussels and limpets), or from archaeological remains (shell middens). All specimen numbers and repository information are shown in Tables 2 and 3, and in Tables S2 and S3. Due to the low proportion of organic matter present in the archaeological shells, the entire valve was used to undertake isotopic analyses. However, samples of the same ages are available to allow the work to be reproducible.

Study site and sample collection

Bones and shells are commonly used in paleontological and archaeological isotopic studies because they contain organic remains and they are often abundant in archaeological deposits as well as in historic museum collections [24], [58], [59], [60]. Furthermore, the proteins they contain integrate the diet over several years [61], [62], [63]. Accordingly, we determined the ratios of stable isotopes of carbon and nitrogen in the organic matrix from the shell of modern and archaeological intertidal mussels (Aulacomya atra atra and Mytilus edulis) and limpets (Nacella magellanica), and in modern and archaeological bone tissue from South American sea lions, South American fur seals and Magellanic penguins. Mussels and limpets were used to characterise the trophic level 1 (herbivores), which allows us to interpret whether shifts in the predators are more likely linked to prey switching or a change in the isotopic baseline. Both modern and archaeological samples were collected in two areas of the South-east coast of South America (Figure 1): central-northern Patagonia (Río Negro and Chubut provinces) and southern Patagonia (Santa Cruz and Tierra del Fuego provinces). These two areas differ in oceanographic, biogeographic and anthropogenic features, with central-northern Patagonia being less productive and more affected by anthropogenic impacts (industrial fishing) than southern Patagonia [64], [65].

Figure 1. Study areas (central-northern Patagonia and southern Patagonia) and sampling approximate zones. Empty dots represent archaeological sites.

Nasal turbinates from modern marine mammal were sampled from specimens at the scientific collections of the Centro Nacional Patagonico (Puerto Madryn, Argentina) and Museo Acatushún (Ushuaia, Argentina) and analysed. Modern penguin bones from adult penguins found dead at breeding colonies distributed along central-northern Patagonia and southern Patagonia were also analysed. Modern mollusc samples were collected from December 2009 to February 2010 at three sites along the coastline of Argentina: two in the Río Negro province (central-northern Patagonia) and one in the Tierra del Fuego province (southern Patagonia) (Figure 1, Table 1).

Sex is often difficult to assess when only fragmented individuals are recovered from the zooarchaelogical record, despite being a major determiner in the foraging habits of fur seals, sea lions and penguins [47], [66], [67], [68], [69]. Accordingly, a sensitivity analysis was run using modern samples from the Río de la Plata region (between southern Brazil and Buenos Aires province) to assess the sensitivity of food web reconstruction using SIBER (see Data analysis). Blue mussels (Mytilus edulis) were collected in the Río de la Plata region to represent ribbed mussel (Aulacomya atra atra), and the limpet Siphonaria lessoni to represent Nacella magellanica (Table 1).

Zooarchaeological bones (generally humeri, mandibles, coxal bones, ribs and femurs) and shell samples recovered from shell middens come from previous fieldwork carried out by Julieta Gómez Otero, Florencia Borrella, Martín Serrán and Lorena Peralta in Golfo de San Matías and Península Valdés (central-northern Patagonia), Eduardo Moreno in Santa Cruz (southern Patagonia) and Ernesto Piana, Luis Orquera, Angie Tivoli and Francisco Zangrando in the Beagle Channel (Tierra del Fuego) (Figure 1, Tables 2 and 3). The samples were dated in different laboratories and using different methods; in particular, in central-northern Patagonia, almost all dated samples were marine shells instead of charcoal. As CO2 diffuses slowly from the atmosphere to the ocean, changes in the abundance of 14C in sea water are delayed in comparison to changes in the atmosphere [70]. Such a lag is known as the reservoir effect and is the responsible for the difference between the radiocarbonic age of coal and shells from the same archaeological level. Reservoir effect data for the central-northern Patagonia region are emerging only recently [71], and they suggest a relatively small difference between marine and terrestrial ages on the basis of a few samples. Although the use of a correction for reservoir effect would be preferable [52], we refer to the conventional, uncalibrated radiocarbon dates for all the sites. This shortcoming should not be of great importance in these types of studies for which precise dates are not required, but large time intervals should suffice.

All samples were stored in a freezer at −20°C until analysis.

Stable isotope analysis

Once in the laboratory, bone and shell samples were thawed and dried in an oven at 50°C, and ground to a fine powder with a mortar and pestle. Shell samples were pre-polished with sandpaper and with a diamond wheel drill to remove impurities. They were subsequently rinsed with distilled water and lipids were extracted in all samples with a chloroform/methanol (2∶1) solution [72].

Since both bone and shell contain high concentrations of inorganic carbon, which may bias δ13C values [73], they were divided into two aliquots. The first was decarbonised by soaking in 0.5 N (bone) or 1 N (shell) hydrochloric acid (HCl) until no more CO2 was released [74]. Since the HCl treatment adversely affects δ15N values [75], the second aliquot was not treated with HCl and used for δ15N determination.

Dried powdered samples and secondary reference standards were combusted at 900°C, and analysed in a continuous flow isotope ratio mass spectrometer (Flash 1112 IRMS Delta C Series EA Thermo Finnigan). For the shell samples, a CO2 absorbent for elemental analyses (CaO/NaOH) was employed to avoid the saturation of the spectrometer during the analysis of the non-acid washed samples, constituted by 90% CaCO3. Stable isotope abundance is expressed in standard δ notation relative to carbonate Pee Dee Belemnite and atmospheric nitrogen. Analyses were performed at the Science and Technology Centre (CCiT) of the University of Barcelona.

Data analysis

Limpets and mussels were analysed together under the “herbivore” category, representing, in the same functional group, both benthic (limpets) and pelagic (mussels) compartments [76]. Each top predator species was analysed separately. Archaeological data were grouped into broad time intervals to enable quantitative reconstruction of food webs. Consequently in central-northern Patagonia all the archaeological samples were pooled together under a single time interval, from 5200±70 yr 14C BP until 380±60 yr 14C BP. This period is entitled the “Pre-contact period” since it predates the arrival of European settlers, opposed to the term post-contact used in archaeology [51], [53], [77]. Ancient samples from southern Patagonia were split in two different periods. The early aboriginal period (EAP) ranging from 6000 to 1100 years ago was characterised by very high oceanic primary productivity [78] and the prevalence of pinnipeds in the economy of hunter-gatherers [50]. Conversely, the late aboriginal period (LAP), ranging from 1000 to 100 years ago, was characterised by a much lower oceanic primary productivity [78] and a lower reliance of the hunter-gatherers economy on pinnipeds. Modern data were analysed separately, so five different food webs were analysed: two in central-northern Patagonia (one archaeological and one modern) and three in southern Patagonia (two archaeological and one modern).

SIBER (Stable Isotope Bayesian Ellipses in R) [79] was used to compute Bayesian Layman's metrics that summarised food web structures in each region and epoch. Only five of the six measures proposed by Layman et al. (2007) [27] were calculated. The δ15N, δ13C ranges (NR and CR, respectively) and the mean distance to centroid (CD) are measures of the total extent of spacing within the δ13C–δ15N bi-plot space and gives a measure of community niche width that is not particularly sensitive to sample size. Nitrogen range (NR) is the representation of the vertical structure of the web; carbon range (CR) gives us an idea of the trophic diversity at the base of the web, while the mean distance to centroid provides a measure of the average degree of trophic diversity within a food web [27]. Mean nearest neighbour distance (MNND) and the standard deviation of nearest neighbour distance (SDNND) reflect the relative position of species to each other within the niche space and can be used to estimate the extent of trophic redundancy.

Furthermore, the overlap (‰) among top predators' standard ellipses corrected for small sample size (SEAC) was calculated in order to analyse resource partitioning among them over time. Comparison of metrics was based on 95% credibility intervals. All codes for SIBER analyses are contained in the package SIAR [80], [81]. Finally, SIBER Bayesian ellipse areas (SEAB) were calculated for the three top predators to measure their isotopic niche width. This approach is similar to a bootstrap, assigning measures of uncertainty, based on Markov-Chain Monte Carlo (MCMC) simulation to construct parameters of ellipses.

In addition, a simulation was performed to test the sensitivity of SIBER metrics to biases in the sex ratio of the top predators. A similar data set from Río de la Plata was used for this analysis (see Table S1). Three different scenarios were simulated: one where only females were included, one where only males were included and a third situation with a balanced sex ratio. These three simulated food webs should represent the three hypothetical and extreme situations emerging from the analysis of the zooarchaeological record, where the sex of the top predators was usually unknown.


The structures of the five food webs analysed are shown in Figure 2. The δ15N values of herbivores decreased from past to present (Table 4) both in central-northern Patagonia (Wilcoxon-Mann-Whitney test: W = 3, p<0.001) and in southern Patagonia (ANOVA: F2,32 = 24.7, p<0.01). Likewise the δ13C values of ancient herbivores from southern Patagonia differed from the modern ones (ANOVA: F2,32 = 5.42, p<0.01) but changes were not statistically significant in central-northern Patagonia (t-test: t = −0.09, df = 16.777, p = 0.93). These results demonstrate that the isotopic baseline may change dramatically throughout time and allow us to properly interpret the structure of the ancient food webs.

Figure 2. Isotopic niches/resource use areas of the species/functional groups described in the text and calculated with the standard ellipse areas corrected for small sample size (SEAC) over time in the two geographical areas.

a) Central-northern Patagonia and b) Southern Patagonia. Herbivores = mussels and limpets; Aa = South American fur seals; Of = South American sea lions; Sm = Magellanic penguins.

Table 4. Mean and standard deviation of nitrogen and carbon stable-isotope in central-northern and southern Patagonia.

The three food webs simulated for the sensitivity analysis did not differ in any of the Layman's metrics (Table 5). The areas of the Bayesian ellipses (SEAB) estimated for the top predators did not either differ among scenarios either, except for fur seals, whose area was maximised when sex ratio was balanced. However, large differences were observed in the overlap between the standard ellipses corrected for small sample size (SEAC) of fur seals and penguins: it ranged from zero when only male fur seals were considered, to 43.73% (fur seals) and 21.34% (penguins) when only females were included. This indicates that the lack of information on the actual sex ratio of ancient data sets is unlikely to bias the overall structure of the food web. Nonetheless caution is needed when interpreting patterns of niche overlap, as they may be sensitive to the sex ratio of the sample.

Table 5. Probability values of Layman's metrics in three simulated model food webs for Río de la Plata region, including only females, males or both sexes in the samples of predators.

The horizontal structure of the food web (CR) did not vary throughout time in central-northern Patagonia but in southern Patagonia the carbon range is currently smaller than in the two past periods considered (Figure 3 and 4). The nitrogen range (NR), indicative of food chain length, increased from past to present in both regions, and did not differ between ancient food webs from southern Patagonia (Figure 3 and 4). Finally, the food webs from southern Patagonia were shorter than those from central-northern Patagonia during the late Holocene as well as in the present.

Figure 3. Probability values of Layman's metrics over the time in the central-northern Patagonia.

Metrics that present differences over the time are indicated by an asterisk and superscripts. Pre = pre-contact period; Mod =  modern period.

Figure 4. Probability values of Layman's metrics over the time in the southern Patagonia.

Metrics that present differences over the time are indicated by an asterisk ad superscripts. Groups sharing the same superscript number (1, 2) are not significantly different. EAP = early aboriginal period; LAP = late aboriginal period; Mod = modern period.

CD and MNND also changed throughout time in both regions, being smaller in the past. This indicates an increase in the trophic diversity and a decrease in the trophic redundancy in modern food webs. Regarding the three species of air predators the areas of the standard ellipses did not overlap in the modern δ13C–δ15N bi-plot space of central-northern Patagonia (Table 6 and Figure 2). Conversely, the topology of the three species within the Pre-contact δ13C–δ15N bi-plot space of the same region departed dramatically from expectations, as the standard ellipses of all the species overlapped one another, especially those of Magellanic penguins and fur seals, in sharp contrast with the low overlap currently observed (Table 6). The topology of the three species in the δ13C–δ15N bi-plot space of southern Patagonia also changed over time, as the overlap among the ellipses of the three species was almost zero in the EAP period (except between sea lions and fur seals where it was 15.38%), increased between penguins and sea lions in the LAP period and is currently about 34% between fur seals and sea lions. Interestingly, the SIBER ellipse areas (SEAB) calculated for each species (Table 7) exhibited a decreasing trend throughout time in central-northern Patagonia, although it was statistically significant only for sea lions. Conversely in southern Patagonia, the sea lions' ellipse area has been constant over time, whereas that of fur seals showed a trend to increase through time and that of penguins slightly increased from the EAP period to the LAP period to then slightly decreased in the present food web (Table 7).

Table 6. Overlap as a percentage of standard ellipses corrected for small samples (SEAc) of the three top predators described in the text.

Table 7. Areas of the estimated Bayesian ellipses of the species/functional groups over the time in central-northern and southern Patagonia.

All the results of the stable isotopes analyses described in the above are publicly available in Table S1S3.


The study of the zooarchaeological record using stable isotope analysis certainly offers a window to explore the structure of ancient food webs, but it is not free from problems. Historical changes in the isotopic baseline are a major shortcoming in retrospective studies using stable isotope analysis to assess changes in trophic level and food web structure [57]. Although widely recognised as a confusing factor, previous studies often assumed the temporal stability of the isotopic baseline [82], [83], [84], [85], [86], [87], [88], [89], but the results reported here demostrate that changes can be dramatic. Post [76] suggested the use of filter feeding mussels and surface-grazing snails as proxies for the baselines of pelagic and littoral aquatic food webs respectively and Bailey and colleagues [88] and Casey and Post [57] recognised the potential of mollusc shells to reconstruct the isotopic baseline in retrospective studies, since their organic matrix is encased within mineral crystals and hence, preserved [90]. The present study demonstrates the potential of the method and offers new perspectives using material that is widely available in paleontological and archaeological collections.

Another drawback from retrospective studies is the uneven distribution of specimens across space and time, which forced us to pool samples of disparate radiocarbon age to reconstruct ancient communities. Uncertainty about the gender of most specimens is another setback of the zooarchaeological record, as sexual secondary characters can seldom be observed. The sensitivity analysis conducted here confirmed the robustness of Layman's metrics to changes in sex ratios of penguins, sea lions and fur seals. Conversely, the overlap between the Bayesian ellipses was highly sensitive to the sex ratio of those species and hence caution is needed when interpreting those results.

The overall evidence reported here indicates that modern marine food webs of central-northern and southern Patagonia are longer (NR) than the ancient ones (Figs 24). Such a conclusion is in sharp contrast with the idea that human exploitation has shortened food webs because of the preferential removal of top predators [4]. Certainly, increased scarcity of large, marine species may have forced fisheries to target smaller species, but there is no reason why surviving top predators had to experience a similar shift. Marine predators are limited by the size of the prey they can consume and draw their energy from a very limited range of trophic levels, in contrast with fisheries [91]. Furthermore, it should be noted that the impact of sealing on the populations of fur seals and sea lions was much larger [39], [40] than that of fishing on the populations of hake, squid and anchovies [20].

Surviving sea lions and fur seals off Argentina have certainly been under carrying capacity during the second half of the 20th century, when the population was less than 10% of the original numbers [39]. This reduced intraspecific competition and led to a major dietary shift in favour of benthic, larger prey with a higher trophic level [24]. Only recently, as the population of sea lions is rebuilding and approaching carrying capacity, sea lions experience resource limitation again and intraspecific competition forces them to increase the consumption of smaller and less profitable prey [92]. Information about the historical dietary changes of South American fur seals is restricted to the last three decades in Río de la Plata and reveals no major dietary changes [93]. However, the population was dramatically reduced during the first half of the 20th century and evidence from other fur seal species in the South-western Atlantic Ocean [94] suggest that this group of smaller and more pelagic pinnipeds also forage at a higher trophic level after severe population declines.

Trophic diversity, measured as the mean distance to the centroid in the isotopic space (CD) also increases in the present food webs, while redundancy (MNND) decreases thus revealing a higher trophic overlap in the past (Figs 24). This was confirmed by the isotopic niche overlap of the three air-breathing top predators, although they differed dramatically in body size and mouth diameter (Table 6). A similar scenario has been reported for waters off Peru, where sea lions, fur seals and penguins primarily rely on the large population of anchoveta Engraulis ringens, supported by intense oceanic productivity [95], [96], [97]. Similarly, a high trophic overlap has often been reported for other wasp-waisted ecosystems in upwelling regions [98]. Currently, a wasp-waist ecosystem supported by amphipods exists off southern Patagonia [99], but amphipods are not consumed directly by fur seals and sea lions. Perhaps a similar wasp-waisted ecosystem supported by small schooling fish might have existed off Patagonia during the Holocene, where primary productivity was usually higher than now [78] and hence it could have supported a larger population of small schooling fish and squids.

However, there are at least two reasons to believe that this is not the explanation for the high levels of overlap and redundancy of the ancient food webs reported here. Firstly, the large population of fur seals inhabiting the highly productive Río de la Plata rely heavily on anchovies and squids [93], but the much smaller sea lion population consumes primarily demersal fishes [100]. Secondly, marine productivity during the late aboriginal period off southern Patagonia was much lower than during the early aboriginal period and closer to actual productivity levels [78], but the structure of the trophic web was indistinguishable from that observed in the same region during the early aboriginal period. Thus, a direct link between productivity, predator diet and the structure of trophic overlap is probably unclear.

Empirical evidence has indicated that marine environments with lower annual temperature variability have smaller predator-prey mass ratios and, consequently, longer food chains [101]. It can be argued that changes in sea water temperature throughout the second half of the Holocene may explain the difference observed between the ancient and modern marine food webs in the South-western Atlantic. However, available evidence rules out major changes in sea surface temperature during the considered time span [51], [55], [102]. Furthermore, there is an inverse relationship between the length of the current food webs and the seasonal variability in the sea surface temperature in the South-western Atlantic [103], a pattern opposite to that reported by Jennings and Warr (2003)[101]. Finally, the difference in the length of the food chain observed between the two areas in both periods is smaller than the difference between periods in both areas.

Thus, human disturbance stands as the most likely reason for the differences in the structure of the food web reported here. Even so, human disturbance is not the only factor explaining the length of marine food webs, as those from southern Patagonia were always shorter and more overlapping than the central-northern Patagonia ones. This might be a consequence of the latitudinal decrease in species diversity reported in the South-western Atlantic [64], [104] and was also probably the reason in the late Holocene, since it is unlikely that the impact of the hunter-gatherers inhabiting central-northern Patagonia on marine resources was larger than that of the hunter-gatherers inhabiting southern Patagonia [51], [52], [53].

In conclusion, this study strongly support the hypothesis that selective exploitation of marine ecosystems, targeting primarily top predators, leads to longer and less overlapping food webs, if top predators are not extinct but survive well below carrying capacity. The situation might be different if human exploitation targeted primarily intermediate trophic levels as a result of the legal protection of top predators.

Furthermore, this study demonstrates the necessity to reconstruct the isotopic baseline in retrospective studies and how this can be achieved by analysing the organic matter encased into the shell of molluscs.

Supporting Information

Table S1.

Modern nitrogen and carbon stable-isotope ratios in Río de la Plata and adjoining areas. These data have been used to perform the sensitivity test for the method.


Table S2.

Modern and archaeological nitrogen and carbon stable-isotope ratios in central-northern Patagonia. Table shows the list of samples, grouped according to their historical period (modern and pre-contact), and δ13C and δ15N values.


Table S3.

Modern and archaeological nitrogen and carbon stable-isotope ratios in southern Patagonia. Table shows the list of samples, grouped according to their historical period (modern, LAP and EAP), and δ13C and δ15N values.



Authors are grateful to Pilar Rubio and Pilar Texidor of the Centres Científics i Tecnològics (CCiT-UB) of the University of Barcelona, where the stable isotope analyses were carried on.

Authors also thank the logistical support provided by the Centro Nacional Patagónico (CENPAT-CONICET) and all the archaeologists who provided the ancient samples: Julieta Gómez Otero, Florencia Borrella, Martín Serrán and Lorena Peralta in Golfo de San Matías and Península Valdés (central-northern Patagonia), Eduardo Moreno, Luis Borrero, Juan Bautista Belardi and Florencia Borella in Santa Cruz (southern Patagonia) and Ernesto Piana, Luis Orquera, Angie Tivoli and Francisco Zangrando in the Beagle Channel (Tierra del Fuego). Finally, the authors wish to acknowledge Maptool program for maps presented in this paper. Maptool is a product of SEATURTLE.ORG (information is available at

Author Contributions

Conceived and designed the experiments: FS LC EAC AA. Performed the experiments: FS DV LS LZ. Analyzed the data: FS SB LC. Contributed reagents/materials/analysis tools: AA LC SB. Contributed to the writing of the manuscript: FS LC SB.


  1. 1. Caddy JF (1998) How pervasive is “fishing down marine food webs”? Science 282: 1383.
  2. 2. Devine JA, Baker KD, Haedrich RL (2006) Fisheries: deep-sea fishes qualify as endangered. Nature 439: 29.
  3. 3. Jackson JB, Kirby MX, Berger WH, Bjorndal KA, Botsford LW, et al. (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293: 629–637.
  4. 4. Pauly D, Christensen V, Dalsgaard J, Froese R, Torres FJ (1998) Fishing down marine food webs. Science 279: 860–863.
  5. 5. Halpern BS, Walbridge S, Selkoe KA, Kappel CV, Micheli F, et al. (2008) A global map of human impact on marine ecosystems. Science 319: 948–952.
  6. 6. Rivadeneira MM, Santoro CM, Marquet PA (2010) Reconstructing the history of human impacts on coastal biodiversity in Chile: constraints and opportunities. Aquatic Conservation: Marine and Freshwater Ecosystems 20: 74–82.
  7. 7. Christensen V, Gue S, Heymans JJ, Walters CJ, Watson R, et al. (2003) Hundred-year decline of North Atlantic predatory fishes. Fish and fisheries 4: 1–24.
  8. 8. Lewison RL, Freeman SA, Crowder LB (2004) Quantifying the effects of fisheries on threatened species: the impact of pelagic longlines on loggerhead and leatherback sea turtles. Ecology Letters 7: 221–231.
  9. 9. Myers RA, Worm B (2003) Rapid worldwide depletion of predatory fish communities. Nature 423: 280–283.
  10. 10. Lotze HK, Coll M, Dunne JA (2011) Historical Changes in Marine Resources, Food-web Structure and Ecosystem Functioning in the Adriatic Sea, Mediterranean. Ecosystems 14: 198–222.
  11. 11. Post DM (2002) The long and short of food-chain length. Trends in Ecology & Evolution 17: 269–277.
  12. 12. Vander Zanden MJ, Fetzer WW (2007) Global patterns of aquatic food chain length. Oikos 116: 1378–1388.
  13. 13. McClenachan L, Cooper AB, Carpenter KE, Dulvy NK (2012) Extinction risk and bottlenecks in the conservation of charismatic marine species. Conservation Letters 5: 73–80.
  14. 14. Worm B, Barbier EB, Beaumont N, Duffy JE, Folke C, et al. (2006) Impacts of biodiversity loss on ocean ecosystem services. Science 314: 787–790.
  15. 15. Dulvy NK, Pinnegar JK, Reynolds JD (2009) Holocene extinctions in the sea. In: Turvey ST, editor. Holocene Extinctions. Oxford: Oxford University Press. pp. 129–150.
  16. 16. Sala E (2004) The Past and Present Topology and Structure of Mediterranean Subtidal Rocky-shore Food Webs. Ecosystems 7: 333–340.
  17. 17. Libralato S, Coll M, Tempesta M, Santojanni A, Spoto M, et al. (2010) Food-web traits of protected and exploited areas of the Adriatic Sea. Biological Conservation 143: 2182–2194.
  18. 18. Kramer DL, Chapman MR (1999) Implications of fish home range size and relocation for marine reserve function. Environmental Biology of Fishes 55: 65–79.
  19. 19. García-Rubies A, Hereu B, Zabala M (2013) Long-Term Recovery Patterns and Limited Spillover of Large Predatory Fish in a Mediterranean MPA. PLoS ONE 8: e73922.
  20. 20. Koen-Alonso M, Yodzis P (2005) Multispecies modelling of some components of the marine community of northern and central Patagonia, Argentina. Canadian Journal of Fisheries and Aquatic Sciences 62: 1490–1512.
  21. 21. Coll M, Navarro J, Olson RJ, Christensen V (2012) Assessing the trophic position and ecological role of squids in marine ecosystems by means of food-web models. Deep Sea Research Part II: Topical Studies in Oceanography: 1–16.
  22. 22. Schweder T (2006) The Scenario Barents Sea study: a case of minimal realistic modelling to compare management strategies for marine ecosystems. In: Boyd I, Wanless S, Camphuysen CJ, editors. Top predators in marine ecosystems Their role in monitoring and management: Cambridge University Press. pp. 310–323.
  23. 23. Chamberlain CP, Waldbauer JR, Fox-Dobbs K, Newsome SD, Koch PL, et al. (2005) Pleistocene to recent dietary shifts in California condors. Proceedings of the National Academy of Sciences of the United States of America 102: 16707–16711.
  24. 24. Drago M, Crespo E, Aguilar A, Cardona L, García N, et al. (2009) Historic diet change of the South American sea lion in Patagonia as revealed by isotopic analysis. Marine Ecology Progress Series 384: 273–286.
  25. 25. Anderson A (2008) Short and sometimes sharp: human impacts on marine resources in the archaeology and history of South Polynesia. In: Erlandson J, Rick TC, editors. Human impacts on ancient marine ecosystems: a global perspective. Berkley: University of California Press. pp. 21–42.
  26. 26. Bearhop S, Adams CE, Waldron S, Fuller RA, Susan EA, et al. (2004) Determining trophic niche width: a novel approach using stable isotope analysis. Journal of Animal Ecology 73: 1007–1012.
  27. 27. Layman CA, Arrington A, Montaña CG, Post DM (2007) Can stable isotope ratios provide for community-wide measures of trophic structure? Comment. Ecology 88: 42–48.
  28. 28. Schmidt SN, Olden JD, Solomon CT, Vander Zanden MJ (2007) Quantitative approaches to the analysis of stable isotope food web data. Ecology 88: 2793–2802.
  29. 29. Schoeninger MJ, DeNiro MJ (1984) Nitrogen and carbon isotopic composition of bone collagen from marine and terrestrial animals. Geochimica et Cosmochimica Acta 48: 625–639.
  30. 30. DeNiro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotope in animals. Geochimica et Cosmochimica Acta 42: 495–506.
  31. 31. DeNiro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochimica et Cosmochimica Acta 45: 41–351.
  32. 32. Arnould JPY (2008) Southern fur seals Arctocephalus spp. In: Perrin WF, Würsig B, Thewissen JGM, editors. Encyclopedia of Marine Mammals. 2nd ed. San Diego: Academic Press. pp. 1079–1084.
  33. 33. Godoy JC (1963) Fauna Silvestre. Buenos Aires: Consejo Federal de Inversiones.
  34. 34. Schiavini A, Crespo EA, Szapkievich V (2004) Status of the population of South American sea lion (Otaria flavescens Shaw, 1800) in southern Argentina. Mammalian Biology 69: 108–118.
  35. 35. Vaz-Ferreira R (1982) Arctocephalus australis, South American fur seal. Mammals in the sea. Rome: FAO Fisheries Series. pp. 497–508.
  36. 36. Vaz-Ferreira R (1982) Otaria flavescens (Shaw) South American sea lion. Mammals in the sea: FAO Fisheries Series. pp. 477–495.
  37. 37. Crespo EA, Pedraza SN (1991) Estado actual y tendencia de la población de lobos marinos de un pelo (Otaria flavescens) en el litoral norpatagónico. Ecología Austral 1: 87–95.
  38. 38. Reyes L, Crespo EA, Szapkievich V (1999) Distribution and population size of the Southern sea lion (Otaria flavescens) in central and southern Chubut, Patagonia, Argentina. Marine Mammal Science 15: 478–493.
  39. 39. Dans SL, Crespo EA, Pedraza SN, Koen Alonso M (2004) Recovery of the South American sea lion (Otaria flavescens) population in northern Patagonia. canadian Journal of Fisheries and Aquatic Sciences 61: 1681–1690.
  40. 40. Túnez JI, Cappozzo HL, Cassini MH (2008) Natural and anthropogenic factors associated with the distribution of South American sea lion along the Atlantic coast. Hydrobiologia 598: 191–202.
  41. 41. Túnez JI, Cappozzo HL, Cassini MH (2008) Regional factors associated with the distribution of South American fur seals along the Atlantic coast of South America. ICES Journal of Marine Science 65: 1733–1738.
  42. 42. Páez E (2006) Situación de la administración del recurso lobos y leones marinos en Uruguay. In: Menafra R, Rodríguez-Gallego L, Scarabino F, Conde F, editors. Bases para la conservación y el manejo de la costa uruguaya. Montevideo: Vida Silvestre, Sociedad Uruguaya para la Conservación de la Naturaleza. pp. 577–583.
  43. 43. Jaureguizar AJ, Milessi AC (2008) Assessing the sources of the fishing down marine food web process in the Argentinean-Uruguayan Common Fishing Zone. Production 72: 25–36.
  44. 44. Dans SL, Koen Alonso M, Crespo EA, Pedraza SN, García NA (2003) Interactions between marine mammals and high seas fisheries in Patagonia: an integrated approach. In: Gales N, Hindell M, Kirkwood R, editors. Marine mammals: fisheries, tourism and management issues. Collingwood: CSIRO Publishing. pp. 100–115.
  45. 45. Vasconcellos M, Csirke J (2011) B6. Southwest Atlantic. FAO-Review of the state of world marine fishery resources. Rome: FAO Fisheries and Aquaculture Technical Paper No. 569. pp. 93–105.
  46. 46. Milessi AC, Jaureguizar AJ (2013) Evolución temporal del nivel trófi co medio de los desembarques en la Zona Común de Pesca Argentino-Uruguaya años 1989-2010. Frente Marítimo 23: 83–93.
  47. 47. Schiavini A, Yorio P, Gandini P, Raya Rey A, Boersma PD (2005) Los pingüinos de las costas argentinas: estado poblacional y conservación. El hornero 20: 5–23.
  48. 48. Boersma DP, Stokes D, Yorio P (1990) Reproductive variability and historical change of Magellan penguin (Spheniscus magellanicus) at Punta Tombo, Argentina. In: Davis LS, Darby JT, editors. Penguin biology. San Diego: Academic Press. pp. 15–43.
  49. 49. Orquera LA, Legoupil D, Piana EL (2011) Littoral adaptation at the southern end of South America. Quaternary International 239: 61–69.
  50. 50. Tivoli AM, Zangrando AF (2011) Subsistence variations and landscape use among maritime hunter-gatherers. A zooarchaeological analysis from the Beagle Channel (Tierra del Fuego, Argentina). Journal of Archaeological Science 38: 1148–1156.
  51. 51. Favier Dubois CM, Borella F, Tykot RH (2009) Explorando tendencias en el uso humano del espacio y los recursos en el litoral rionegrino durante el Holoceno tardío y medio. In: Salemme MC, Santiago M, Alvarez M, Piana EL, Vázquez M, et al., editors. Holocene. Ushuaia: Editorial Utopía. pp. 985–998.
  52. 52. Gómez Otero J (2006) Dieta, uso del espacio y evolución en sociedades cazadoras-recolectoras de la costa centro- septentrional de Patagonia durante el Holoceno medio y tardío. [PhD thesis]. Buenos Aires: Universidad de Buenos Aires.
  53. 53. Gómez Otero J (2007) Isótopos estables, dieta y uso del espacio en la costa atlántica centro-septentrional y el valle inferior del río Chubut (Patagonia, Argentina). In: Morello F, Martinic M, Prieto A, Bahamond G, editors. Arqueología de Fuego-Patagonia Levantando piedras, desenterrando huesosy develando arcanos. Punta Arenas, Chile: CEQUA. pp. 151–161.
  54. 54. Moreno E (2008) Arqueología y etnohistoria de la costa patagónica central en el Holoceno tardío.: Fondo Editorial Provincial, Secretaría de Cultura del Chubut.
  55. 55. Saporiti F, Bala LO, Crespo EA, Gómez Otero J, Zangrando AFJ, et al. (2013) Changing patterns of marine resource exploitation by hunter-gatherers throughout the late Holocene of Argentina are uncorrelated to sea surface temperature. Quaternary International 299: 108–115.
  56. 56. Zangrando FA, Panarello H, Piana EL (2013) Zooarchaeological and Stable Isotopic Assessments on Pinniped-human Relations in the Beagle Channel (Tierra del Fuego, Southern South America). International Journal of Osteoarchaeology 24: 231–244.
  57. 57. Casey MM, Post DM (2011) The problem of isotopic baseline: Reconstructing the diet and trophic position of fossil animals. Earth-Science Reviews 106: 131–148.
  58. 58. Newsome SD, Clementz MT, Koch PL (2010) Using stable isotope biogeochemistry to study marine mammal ecology. Marine Mammal Science 26: 509–572.
  59. 59. O'Donnell TH, Macko SA, Chou J, Davis-Hartten KL, Wehmiller JF (2003) Analysis of δ13C, δ15N, and δ34S in organic matter from the biominerals of modern and fossil Mercenaria spp. Organic Geochemistry 34: 165–183.
  60. 60. Versteegh EAA, Gillikin DP, Dehairs F (2011) Analysis of δ15N values in mollusk shell organic matrix by elemental analysis/isotope ratio mass spectrometry without acidification: an evaluation and effects of long-term preservation. Rapid communications in mass spectrometry: RCM 25: 675–680.
  61. 61. Hilderbrand GV, Farley SD, Robbins CT, Hanley TA, Titus K, et al. (1996) Use of stable isotopes to determine diets of living and extinct bears. Canadian Journal of Fisheries and Aquatic Sciences 74: 2080–2088.
  62. 62. Hobson KA, Clark RG (1992) Assessing avian diets using stable isotopes I: turnover of 13C in tissues. The Condor 94: 181–188.
  63. 63. Jones D, Quitmyer I (1996) Marking time with bivalve shells: oxygen isotopes and season of annual increment formation. Palaios 11: 340–346.
  64. 64. Cousseau MB, Perrotta RG (2000) Peces marinos de Argentina. biología, distribución, pesca. Mar del Plata: INIDEP.
  65. 65. Piola A, Falabella V (2009) El Mar Patagónico; Falabella V, Claudio C, Croxal J, editors. Buenos Aires: Wildlife Conservation Society y BirdLife International.
  66. 66. Koen Alonso M, Crespo EA, Pedraza SN, García N, Coscarella MA (2000) Food habits of the South American sea lion, Otaria flavescens, off Patagonia, Argentina. Fishery bulletin 98: 250–263.
  67. 67. Page B, McKenzie J, Goldsworthy SD (2005) Dietary resource partitioning among sympatric New Zealand and Australian fur seals. Marine Ecology Progress Series 293: 283–302.
  68. 68. Drago M, Cardona L, Crespo EA, Aguilar A (2009) Ontogenic dietary changes in South American sea lions. Journal of Zoology 279: 251–261.
  69. 69. Silva L, Saporit F, Vales D, Tavares M, Gandini P, et al. (2014) Differences in diet composition and foraging patterns between sexes of the Magellanic penguin (Spheniscus magellanicus) during the non-breeding period as revealed by δ13C and δ15N values in feathers and bone. Marine Biology 161: 1195–1206.
  70. 70. Mangerud J (1972) Radiocarbon dating of marine shells, including a discussion of apparent ages of Recent shells from Norway. Boreas 1: 143–172.
  71. 71. Favier Dubois CM (2009) Valores de efecto reservorio marino para los últimos 5.000 años obtenidos en concheros de la costa atlántica norpatagónica (Golfo san Matías, Argentina). Magallania 37: 139–147.
  72. 72. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology 37: 911–917.
  73. 73. Lorrain A, Savoye N, Chauvaud L, Paulet Y-M, Naulet N (2003) Decarbonation and preservation method for the analysis of organic C and N contents and stable isotope ratios of low-carbonated suspended particulate material. Analytica Chimica Acta 491: 125–133.
  74. 74. Newsome SD, Koch PL, Etnier MA, Aurioles-Gamboa D (2006) Using carbon and nitrogen isotope values to investigate maternal strategies in northeast Pacific otariids. Marine Mammal Science 22: 556–572.
  75. 75. Bunn SE, Loneragan NR, Kempster MA (1995) Effects of acid washing on stable isotope ratios of C and N in penaeid shrimp and seagrass: implications for food-web studies using multiple stable isotopes. Limnology and Oceanography 40: 622–625.
  76. 76. Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83: 703–718.
  77. 77. Moreno E, Zangrando AF, Tessone A, Castro A (2011) Isótopos estables, fauna y tecnología en el estudio de los cazadores-recolectores de la costa norte de santa cruz. MAGALLANIA, (Chile) 39: 265–276.
  78. 78. Saporiti F, Bala LO, Gómez Otero J, Crespo EA, Piana E, et al. (unpublished) Paleoindian pinniped exploitation in South America was driven by oceanic productivity Quaternary International.
  79. 79. Jackson AL, Inger R, Parnell AC, Bearhop S (2011) Comparing isotopic niche widths among and within communities: SIBER - Stable Isotope Bayesian Ellipses in R. The Journal of animal ecology 80: 595–602.
  80. 80. Parnell A, Jackson A (2013) SIAR: Stable Isotope Analysis in R.
  81. 81. Parnell AC, Inger R, Bearhop S, Jackson AL (2010) Source partitioning using stable isotopes: coping with too much variation. PloS one 5: e9672.
  82. 82. Burton R, Snodgrass J, Gifford-Gonzalez D, Guilderson T, Brown T, et al. (2001) Holocene changes in the ecology of northern fur seals: insights from stable isotopes and archaeofauna. Oecologia 128: 107–115.
  83. 83. Wainright SC, Fogarty MJ, Greenfield RC, Fry B (1993) Long-term changes in the Georges Bank food web: trends in stable isotopic compositions of fish scales. Marine Biology 115: 481–493.
  84. 84. Emslie SD, Patterson WP (2007) Abrupt recent shift in d13C and d15N values in Adélie penguin eggshell in Antarctica. Proceedings of the National Academy of Sciences of the United States of America 104: 11666–11669.
  85. 85. Becker BH, Beissinger SR (2006) Centennial Decline in the Trophic Level of an Endangered Seabird after Fisheries Decline. Conservation Biology 20: 470–479.
  86. 86. Christensen J, Richardson K (2008) Stable isotope evidence of long-term changes in the North Sea food web structure. Marine Ecology Progress Series 368: 1–8.
  87. 87. Corbett A, Causey D, Clementz M, Koch PL, Doroff A, et al. (2008) Aleut hunters, sea otters, and sea cows. In: Rick TC, Erlandson JM, editors. Human impacts on ancient marine ecosystems. Berkley: University of California Press. pp. 43–75.
  88. 88. Bailey G, Barrett J, Craig O, Milner N (2008) Historical ecology of the North Sea basin: an archaeological perspective and some problems of metodology. In: Rick TC, Erlandson JM, editors. Human impacts on ancient marine ecosystems: University of California Press. pp. 215–242.
  89. 89. Barrett J, Johnstone C, Harland J, Van Neer W, Ervynck A, et al. (2008) Detecting the medieval cod trade: a new method and first results. Journal of Archaeological Science 35: 850–861.
  90. 90. Crenshaw MA (1980) Mechanisms of shell formation and dissolution. In: Rhoads DC, Lutz RA, editors. Skeletal growth of aquatic organisms. New York: Plenum Press. pp. 115–132.
  91. 91. Trites A, Christensen V, Pauly D (2006) Effects of fisheries on ecosystems: just another top predator? In: Boyd I, Wanless S, Camphuysen C, editors. Top Predators in Marine Ecosystems: Cambridge University Press. pp. 11–27.
  92. 92. Drago M, Cardona L, Crespo EA, Grandi M, Aguilar A (2010) Reduction of skull size in South American sea lions reveals density-dependent growth during population recovery. Marine Ecology Progress Series 420: 253–261.
  93. 93. Vales DG, Saporiti F, Cardona L, De Oliveira LR, Dos Santos RA, et al. (2013) Intensive fishing has not forced dietary change in the South American fur seal Arctophoca( = Arctocephalus)australis off Río de la Plata and adjoining areas. Aquatic Conservation: Marine and Freshwater Ecosystems: n/a-n/a.
  94. 94. Hanson N, Wurster C, Bird M, Reid K, Boyd I (2009) Intrinsic and extrinsic forcing in life histories: patterns of growth and stable isotopes in male Antarctic fur seal teeth. Marine Ecology Progress Series 388: 263–272.
  95. 95. Muck P, Fuentes H (1987) Sea lion and fur seal predation on the Peruvian anchoveta, 1953 to 1982. In: Pauly D, Tsukuyama I, editors. The peruvian anchoveta and its upwelling ecosystem: three decades of change: ICLARM studies and Reviews. pp. 351.
  96. 96. Soto KH, Trites AW, Arias-Schreiber M (2004) The effects of prey availability on pup mortality and the timing of birth of South American sea lions (Otaria flavescens) in Peru. Journal of Zoology 264: 419–428.
  97. 97. Herling C, Culik BM, Hennicke JC (2005) Diet of the Humboldt penguin (Spheniscus humboldti) in northern and southern Chile. Marine Biology 147: 13–25.
  98. 98. Cury P, Bakun A, Crawford RJM, Jarre A, Quiñones RA, et al. (2000) Small pelagics in upwelling systems: patterns of interaction and structural changes in “wasp-waist” ecosystems. ICES Journal of Marine Science 57: 603–618.
  99. 99. Padovani LN, Viñas MD, Sánchez F, Mianzan H (2012) Amphipod-supported food web: Themisto gaudichaudii, a key food resource for fishes in the southern Patagonian Shelf. Journal of Sea Research 67: 85–90.
  100. 100. Riet-Sapriza FG, Costa DP, Franco-Trecu V, Marín Y, Chocca J, et al. (2013) Foraging behavior of lactating South American sea lions (Otaria flavescens) and spatial–temporal resource overlap with the Uruguayan fisheries. Deep Sea Research Part II: Topical Studies in Oceanography 88–89: 106–119.
  101. 101. Jennings S, Warr KJ (2003) Smaller predator–prey body size ratios in longer food chains. Proceedings of the Royal Society Biological Sciences 1413–1417.
  102. 102. Obelic B, Álvarez A, Argullós J, Piana EL (1998) Determination of water palaeotemperature in the Beagle Channel (Argentina) during the last 6000 yr through stable isotope composition of Mytilus edulis shells. Quaternary of South America and Antarctic Peninsula 11: 47–71.
  103. 103. Rivas AL (2010) Spatial and temporal variability of satellite-derived sea surface temperature in the southwestern Atlantic Ocean. Continental Shelf Research 30: 752–760.
  104. 104. Balech E, Ehrlich MD (2008) Esquema biogeográfico del Mar Argentino. Revista de investigación y desarrollo pesquero. 19: 45–75.
  105. 105. Gómez Otero J, Suárez F (1999) Lobos marinos y guanacos: análisis arqueofaunístico de un fogón hallado en la costa del Golfo de San Matías, Península Valdés (Chubut). Resúmenes del XIII Congreso Nacional de Arqueología Argentina: Universidad de Córdoba. pp. 396.
  106. 106. Serrán M, Centeno N, Weiler N, Gómez Otero J (2008) Massive death of pinnipeds 1200 years ago: taphonomic history of the “Lobos site” (Golfo Nuevo, Patagonia, Argentina). Quaternary International 183: 135–142.
  107. 107. Schiavini A (1993) Los lobos marinos como recurso para cazadores-recolectores marinos: el caso de Tierra del Fuego. Latin American Antiquity 4: 346–366.
  108. 108. L'Heureux G, Franco NV (2002) Ocupaciones humanas en el área de cabo Vírgenes (Pcia de Santa Cruz, Argentina): el sitio Cabo Vírgenes 6. Anales del Instituto de la Patagonia (Serie Ciencias Humanas) 30.
  109. 109. Beretta M, Corinaldessi L, Castro A (2011) Recursos marinos vs. recursos terrestres: análisis arqueofaunístico en el sitio Cueva del Negro, costa norte de Santa Cruz. Arqueología 17: 137–159.
  110. 110. Orquera L, Piana E (1987) Composición tipológica y datos tecnomorfológicos y tecnofuncionales de los conjuntos arqueológicos del sitio Túnel I (Tierra del Fuego, República Argentina). Relaciones de la Sociedad Argentina de Antropología 17: 201–239.
  111. 111. Piana E, Vázquez M, Ceraso A (2007) Kaiyawoteha. Informe de excavación. Ushuaia.
  112. 112. Belardi JB, Carballo Marina F, L'Heureux GL (2011) Nuevos resultados arqueológicos en Cabo Vírgenes (Santa Cruz, Argentina): el sitio Cabo Vírgenes 20. Magallania, (Chile) 39: 279–292.
  113. 113. Tivoli AM (2010) Las aves en la organización socioeconómica de cazadores-recolectores-pescadores del extremo sur sudamericano. Buenos Aires: Universidad de Buenos Aires.
  114. 114. Orquera L, Piana E (1997) El sitio Shamakush I. Relaciones. Relaciones de la Sociedad Argentina de Antropología 21: 215–265.