Archaeological sharks: Late Holocene changes in trophic ecology and habitat use of sharks in South Brazil

doi:10.21203/rs.3.rs-2719805/v1

Download PDF

Research Article

Archaeological sharks: Late Holocene changes in trophic ecology and habitat use of sharks in South Brazil

https://doi.org/10.21203/rs.3.rs-2719805/v1

This work is licensed under a CC BY 4.0 License

Journal Publication

published 05 Jul, 2023

Read the published version in Marine Biology →

You are reading this latest preprint version

Sharks are essential components of marine food webs, but their removal might simplify ecosystems and food webs. Comparing the isotopic niche of species between archaeological and modern communities can provide information to assess temporal changes in the ecological dynamics of communities. Here, stable isotope analysis was used to compare food web topology metrics between two shark guilds or communities, a late Holocene archaeological community (AC) dating from 724 − 542 years ago and a modern community (MC) trophic web, both from South Brazil. In the same line of comparison, we assess the trophic position of a top predator, Carcharias taurus. Results showed topological temporal differences such as higher trophic redundancy and higher patterns of niche overlap in the AC. Higher trophic redundancy could be expected in late Holocene food webs, as similar studies also observed these findings. In contrast, the MC showed dispersion of species throughout the isotopic space, thus higher niche partitioning and higher trophic diversity, suggesting changing ecological interaction dynamics. We found that Carcharias taurus has increased its trophic level, possibly due to a release from the intraspecific competition and a dietary shift towards larger prey items. We suggest that anthropic impacts, such as overfishing, may cause these differences in the trophic position of this species. We also advocate that this study method might help future trophic reconstructions using shark teeth, as information about past marine environments is scarce, and could serve as a baseline for future studies.

Historical ecology

Isotopic niche

Anthropic impacts

Topology

Trophic level

Humans are catalyzing changes in marine ecosystems through accelerating climate change, pollution, habitat degradation, facilitation of invasive species and causing the collapse of many fisheries, leading to biodiversity loss and impairment of ecosystems structure and functions (Worm et al. 2006; Doney et al. 2012). Some of these impacts started millennia ago, consequently, many ecosystems as seen today functioned differently in the past (Jackson et al. 2001). As a result, both historically and recently, human impacts caused regime shifts and changed well-established ecosystem dynamics, trophic interactions, and many other ecological aspects in marine ecosystems (Jackson et al. 2001; Erlandson and Rick 2008; Maureaud et al. 2017). In this anthropic context, the original trophic ecology of many species almost certainly was not preserved over the years (e.g. Saporiti et al. 2014; Vales et al. 2017; Bas et al. 2019).

Sharks are a group of highly diverse marine predators inhabiting a wide range of habitats in all oceans (Ebert et al. 2013). It is estimated that more than 1/3 species of Chondrichthyes are threatened according to the IUCN red list (Dulvy et al. 2021). Among these, sharks are of special concern, due to population declines on a global scale over the last century, largely because of overfishing and habitat loss (Ferretti et al. 2010; Worm et al. 2013; Dulvy et al. 2021; Pacoureau et al. 2021). This general scenario is not different for shark populations in the South Atlantic, as off the southern Brazilian coast, shark populations are currently depleted by longline fisheries (Barreto et al. 2016).

Due to their life-history traits, such as late maturity, slow growth and low reproductive rates, shark populations are highly sensitive to changes in survival rates (Ferretti et al. 2010). As such, sharks are not resilient to negative pressures and therefore their declines often have consequences in many ecological scales. Broad ecological consequences include trophic cascades, mesopredator release and consequently indirect changes in trophic interactions (Myers et al. 2007; Baum and Worm 2009). While in small scales, removing individual species can lead to changes in relative abundances, life-history parameters, populations size structure, reduced competition and predation intensity for other sharks (Pauly 1988; Ferretti et al. 2010). More simply, sharks removal or declines ultimately simplify oceanic ecosystems (Baum and Worm 2009). Therefore, investigating only the current trophic ecology may not be reliable indicators to the original trophic ecology of sharks in any environment under the influence of heavy anthropic impacts.

To address temporal ecological questions and to reconstruct the trophic ecology of species before modern anthropic impacts, stable isotopes analysis (SIA) of carbon and nitrogen are reliable tools (e.g. Drago et al. 2017; Vales et al. 2017). One of the advantages of SIA is the application in animal bone to assess the isotopic composition in collagen, and consequently further use on museum or prehistoric material, allowing reconstructions of historical food webs. Bone collagen have shown to be very resistant to diagenetic effects, even in Pleistocene bone remains (Dobberstein et al. 2009).

The archaeological context from South Brazil provides an opportunity to study trophic ecology of sharks before major anthropic impacts. Archaeological elasmobranch remains, such as teeth and vertebrae, are ubiquitous in archaeological faunal assemblages of southeastern and southern Brazilian coast (Lopes et al. 2016; Mendes et al. 2018; Burg Mayer et al. 2022)—shark teeth and vertebrae stand out due to their highest degree of calcification (Reitz and Wing 2008). SIA in shark teeth provide a singular time integrated dietary isotopic values referent to when teeth begin and end its formation, absorbing into its collagen diet-related stable isotopes from blood aminoacids (Zeichner et al. 2017). Therefore, stable isotopes from shark teeth represents an integrated diet signal composition from weeks to months, and not a whole life average.

The archaeological record evidence well-developed prehistoric fisheries targeting sharks and rays and shows an exploitation of neonates and juveniles sharks and rays, and suggests an early stage of overexploitation of some medium to large size fish species (Lopes et al. 2016). Records from southeastern and southern Brazil show high shark diversity and the presence of nowadays rare species at the Brazilian coast (e.g. great white shark, Carcharodon carcharias) and species currently with highly reduced populations (e.g. sand tiger shark, Carcharias taurus; ICMBio 2018) and many other shark species (Lopes et al. 2016; Mendes et al. 2018; Burg Mayer et al. 2022).

As such, major changes in the local and regional marine communities occurred. C. taurus, one the most abundant shark remains in Brazilian archaeological shellmounds (e.g. Lopes et al. 2016; Mendes et al. 2018; Burg Mayer et al. 2022), also was historically abundant in the South of Brazil, the species was so abundant that beach trawl fishing caught schools of this shark (Vooren and Klippel 2005). However, as many other shark species of South Brazil, their populations were heavily exploited in the last decades (Kotas 2005; Santos 2020), suggesting currently depleted populations, with unknown consequences to their trophic ecology. Besides, there is no information about the trophic ecology of local sharks before population depletion. Despite several worldwide studies about the ecological consequences of shark population declines, the impacts of these declines remain uncertain (Heithaus et al. 2008, Roff et al. 2016).

Therefore, in this study, we use a historical approach to describe and compare the isotopic niche ecology (isotopic topology, isotopic niche variation, and overlap) of a modern community (MC) of sharks to an archaeological community (AC) of sharks from the late Holocene. We also assess the trophic position of C. taurus in light of this comparison and discuss the potential role of human impacts in changing the trophic ecology of this species.

Study area and sampling

Archaeological shark teeth were obtained from Rio do Meio site, a shallow site (a shellmound variation) in South Brazil (Fig. 1), located at the north of the island of Santa Catarina, on Jurere beach, at 27°26'23"S, 48°29'56"W (Fossari 2004). The site dates around 724 − 542 years cal.B.P. (calibrated, before present; Fossari 2004).

Before anthropic interference in area which caused the burial of the site, Rio do Meio site was parallel to Jurere beach coastline, under dunes which were fixated by sandbank vegetation and near a body of estuarine water (Fossari 2004). This site is surrounded by mangrove to the South and neoproterozoic granite rock mounds to East and West (Fossari 2004).

This study site is at the Southern Brazil shelf (27°S), extending from latitude 34ºS to 22ºS and characterized as a subtropical temperate environment and by a narrow continental shelf (Mahiques et al. 2010) and conspicuous seasonality effects on sea surface temperature and chlorophyll concentration (Pereira et al. 2009). This section of the shelf is on a transition zone, which lies within the path of the southward flowing Brazil current, dominated by estuarine outflows, and the northward flowing Maldivas current (Piola et al. 2000; Heileman and Gasalla 2009). The primary productivity is highly influenced by terrigenous input, and is affected by cold waters intrusions from the subtropical confluence zone and by the plume carrying sediments originating from La Plata estuary, which might go up to 28°S (Mahiques et al. 2010).

Except for variations in the strength of the Brazil Current (Chiessi et al. 2014) between the latest site datation (724 years cal.B.P.) up to recent times, there were no major changes in oceanographic conditions in the Southern Brazil Shelf (Mahiques et al. 2009; Nagai et al. 2014).

The archaeological site collection is housed at the Museum of Archeology and Ethnology Oswaldo Rodrigues Cabral (MArquE) at Federal University of Santa Catarina (UFSC) campus in Florianópolis.

To taxonomically identify the faunal remains of sharks, and to reduce pseudo replication and misidentifications, we followed the same criteria as in Burg Mayer et al. (2022).

To minimize sampling different class sizes or juveniles for Carcharhinus and other considered species, only archaeological teeth with a specific crown height size range were sampled for SIA (Online Resource 1).

Modern samples of shark teeth specimens, within the size range specified above, were obtained from UNIVALI Oceanographic Museum collection. Specimens from this collection were collected along southern Brazil coast, mainly at the state of Santa Catarina, from 1980 to 2010. These include C. plumbeus (N = 6), C. brachyurus (N = 6), C. obscurus (N = 6), C. taurus (N = 10), C. carcharias (N = 1), G. cuvier (N = 1), I. oxyrhinchus (N = 9), C. brachyurus (N = 3), C. leucas (N = 2) and G. cuvier (N = 1; Online Resource 2). Both archaeological and modern samples from museums were dry stored for later analysis.

To assess the habitat use and validate δ¹³C values for some species of interest, we considered the classification provided by Fishbase (Froese and Pauly 2018) regarding the species habitat use. Following this classification we attributed modern and archaeological C. taurus δ¹³C values to be representative of a reef-associated environment.

Sample preparation and methodological adaptations

Shark teeth were washed with distilled water and cleaned of external debris with a sandpaper. Samples were then dried at 50 ºC for 6 hours before powder extraction. The outer layer of the shark teeth is mostly enameloid, a coarsely crystalline matrix which contains relative low organic material (~ 5%), whereas the inside of teeth is mostly finer grained dentin, containing more organic matrix (15%-20%), mainly collagen (LeGeros 1981; Kemp 1984; Enax et al. 2012), that captures the isotopic signal of diet (Vennemann et al. 2001). Therefore, disregarding the enameloid, we extracted dentin to a fine powder using a low-speed cutting drill with bits ranging in size from 800 to 1500 mm.

The choice of using EDTA to decalcify shark teeth powder is explained in Online Resource 1. 1.5 mL of 0.5 M EDTA (pH 8) was added and vortexed to each powdered tooth sample and left to react for one week at room temperature. Once samples were visibly demineralized, as evidenced by a translucent powder, they were centrifuged (8 minutes at 12,000 rpm), the supernatant removed with a pipette. Then samples were vortexed for 30 seconds embedded in MilliQ deionized water and centrifuged again. This was repeated 11 times, in the 5th and the 10th time the samples were left soaked overnight (adapted from Kim and Koch 2012) Samples were freeze-dried before enclosing approximately 1.5 mg of material into tin cups for isotopic analysis, which is specified in Online Resource 1.

Data Analysis

Prior to analysis and when applicable, data were checked for normality using Lilliefors and Shapiro (less than four samples) test, and checked for homogeneity of variance using Levene’s test and diagnostic plots in R (R Development Core Team 2018).

C:N ratios were considered to assess the general preservation state of bone collagen, usually, C:N ratios between 2:9 − 3:6 are indicative of well-preserved bone collagen ratios or collagen without contaminants (DeNiro 1985). Nevertheless, these ratios are mostly used to check bone collagen integrity for mammals and bony fish (see Szpak 2011). Given the inherently different nature of shark teeth ontogeny from bony fish and mammalian bone, and the lower ratios of C:N in fresh collected shark tooth (Zeichner et al. 2017), samples found at lower C:N ratios (2:6 − 2:7) were included in the analysis.

We performed Student t-tests for independent samples for normally distributed data to compare habitat use for C. taurus between communities.

The package SIBER (Stable Isotope Bayesian Ellipses in R; Jackson et al. 2011) was used to calculate and compare for each shark species with a minimum sampling (N ≥ 3) in both periods, the convex hull or total area (TA), and two estimates for the standard ellipse area: SEAc and SEAb. SEAb is the Bayesian standard ellipse area, and is reported as median values and 95% credible intervals, whereas the SEAc is the small sample corrected ellipse area with no associated errors. SEAc and SEAb are calculated from the variance and covariance of bivariate data and contains approximately 40% of the data, thus they reveal the core niche area and are expected to be insensitive to sample size (Jackson et al. 2011).

SIBER package also was used to compute the Bayesian Layman’s metrics for each of the time-separated food web communities (Layman et al. 2007; Jackson et al. 2011) and further comparison between communities. These isotopic metrics are proxies for the trophic structure of a given community using a dual isotopic approach (δ¹³C-δ¹⁵N), and are calculated based on the distribution and dispersion of species in the δ-space. Five of six of the Layman’s metrics were calculated. The δ¹⁵N range (NR) is a representation of the length of the food web and is the distance between the two species with the most enriched and most depleted δ¹⁵N values, generally, a larger range in δ¹⁵N among consumers suggests more trophic levels or a more trophic diversity food web. The δ¹³C range (CR) represents the width of the food web and indicates the various sources of carbon pool driving the food web. The mean distance to centroid (CD) better represents the average degree of trophic diversity within a food web (Layman et al. 2007), as it is unbiased in the case where outliers inflates NR or CR. The CD is measured as the mean Euclidean distance to the centroid estimated from the average Euclidean distance from each species to the centroid of the food web. The mean nearest neighbor distance (NND) represents the trophic redundancy of the food web, as the overall density of species packing within the isotopic niche space. While the standard deviation of nearest neighbor distances (SDNND) represents the overall functional evenness of individual species packing (Layman et al. 2007). Layman’s metrics have been recently being categorized as ‘isotopic functional indices’, because they can serve as proxies to the metrics developed by functional ecologists (Belle and Cabana 2020). These isotopic functional indices can be coupled into groups: isotopic functional richness (CR, NR, and TA), isotopic functional divergence (CD) and isotopic functional evenness (NND, SDNND). In this analysis, only same taxa from both communities with the minimum number of samples were used (C. taurus, C. plumbeus, C. leucas, Isurus oxyrinchus and Carcharhinus brachyurus). We then removed each species from the analysis to test their effect on the metrics results. We tested the posterior distributions of the Layman’s metrics between communities by pairwise comparison tests (using the approach delineated in SIBER; Jackson et al. 2011). These test the probability that one metric differs from the other (being higher or lower). The results are expressed in confidence probability (e.g. prob = 0.96, a 96% probability).

Shark size was estimated based on teeth regressions equations available for C. taurus and C. carcharias, giving results in total length (TL, cm; Shimada 2003, 2004). Shark teeth position in the jaw was estimated based on compared morphology for C. taurus. For modern species with no TL data available, we measured the crown height from second upper tooth directly from their jaws for size regression (Shimada 2003, 2004). To proceed with a padronized by size trophic position analysis, we separated data of C. taurus in similar size classes among archaeological and modern species. Size regression estimates indicates that archaeological C. taurus ranged from 232 to 274 cm (mean 253.6; N = 9), modern C. taurus ranged from 223–273 cm (mean 248.3; N = 7). To make inferences about the trophic ecology of C. carcharias, we also calculated its estimated TL, which ranged from 216–315 (mean 262.9; N = 5).

We only used C. taurus for the trophic position analysis because size regression equations were only available for this species with minimal sample size in both communities. It is important to standardize size in trophic position analysis, as bigger fish could result in elevated δ¹³C and δ¹⁵N values, due to ontogenetic shifts or feeding niche differences among size classes (e.g. Estrada et al. 2006) and also because trophic level correlates with body size (Jennings 2005).

We calculated the trophic position (TP) for C. taurus using the package ‘tRophicposition’ for R environment, a Bayesian approach that uses Markov Chain Monte Carlo Simulations coupled with stable isotope data and the mean and standard deviation for trophic discrimination factors (TDF; Quezada-Romegialli et al. 2018). Unlike trophic level, TP recognizes that species might feed in multiple trophic levels, hence it may become fractional (Zander and Rasmussen 1996). A prior for the parameter TP was set to a normal distribution of mean of 4.4 (for C. taurus) and standard deviation of 0.1, as defined by stomach content analysis (Cortés 1999). TDF values and standard deviations of Δ¹³C and Δ¹⁵N for shark teeth were obtained from Zeichner et al. (2017) and used to generate a normal distribution (N = 1000). TP must be calculated relative to a baseline (primary or secondary consumers) of the organism respective food-chain (Hussey et al. 2012a). Secondary consumer baselines values for the archaeological species were obtained from premaxilar bone collagen of Micropogonias furnieri, from the same archaeological site as this study, and it was considered at a TP of 3 (Milessi et al. 2005). Baselines from MC were obtained from the mussel Mytilus edulis (TP = 2; Caut et al. 2009), collected in the years of 1988 and 2014 along the coast of Uruguay and Rio Grande do Sul state, Brazil (Drago et al. 2017). For C. taurus in each community, 20000 iterations were run across Markov Chains to generate TP estimations. The results generated posterior density distribution with associated 95% credible intervals. Similar to the Layman’s metrics, we performed pairwise tests in the posterior distributions for differences in the trophic position. The regressed size data were normally distributed.

Variation in C:N ratios and δ¹³C - δ¹⁵N

Overall, 50 archaeological shark teeth belonging to nine species were selected and analyzed (Online Resource 3), whereas 47 samples from modern samples were obtained for analysis, belonging mainly to nine species (Online Resource 2). For the archaeological samples, 29 out of 50 samples C:N ranges lay within the expected value for well-preserved bone collagen ratios (2:9 − 3:6), and the other 21 samples lay within 2.7–2.8 ratios. Samples of C:N ratio > 3.6 were excluded from the analysis.

Average δ¹³C ranged from − 10.9‰ to -12.9‰ for the AC and − 11.0‰ to -13.5‰ for MC (Table 1). The most ¹³C enriched species for δ¹³C in both communities were C. taurus, whereas the least δ ¹³C enriched were Isurus and G. cuvier (Table 1).

Table 1

Stable isotopes values (δ¹³C and δ¹⁵N), sample sizes (N) and standard ellipse areas and total areas for both archaeological and modern communities. SEAc is the ellipse area corrected for small sample sizes; SEAb is the Bayesian estimation of the ellipse area, values in brackets show 95% credible intervals; TA: total area of the convex hull; Cal.B.P is the calibrated datation before present.
Species	Period	N	δ13C ± SD	δ15N ± SD	SEAc	SEAb	TA
Sandtiger shark (Carcharias taurus)	724 − 542 years cal.B.P.	14	-10.84 ± 0.53	17.37 ± 1.29	2.35	2.16 [0.92–2.89]	4.57
	Present	10	-11.0 ± 1.20	18.5 ± 0.70	2.8	2.5 [1.07–4.5]	4.19
Requiem shark (Carcharhinus plumbeus)	724 − 542 years cal.B.P.	6	-11.11 ± 0.96	15.41 ± 1.10	1.67	1.34 [0.94–5.95]	1.74
	Present ◦	6	-12.4 ± 0.82	13.6 ± 2.4	7	5.6 [1.02–6.03]	6.53
Cooper shark (Carcharhinus brachyurus)	724 − 542 years cal.B.P.	4	-11.45 ± 0.62	16.52 ± 1.04	2.99	1.99 [0.51–5.66]	1.45
	Present	6	-12.25 ± 0.67	16.00 ± 1.54	3.79	3.03 [0.96–8.38]	3.56
Dusky shark (Carcharhinus obscurus)	Present	6	-11.7 ± 1.35	14.23 ± 1.37	6.55	5.24 [1.87–12.33]	7.36
Mako sharks (Isurus paucus▫ and Isurus oxyrhinchus▪)	724 − 542 years cal.B.P. ▫	4	-12.42 ± 1.73	15.10 ± 1.09	8.53	5.69 [0.86–13.31]	5.41
	Present ▪	15	-13.16 ± 0.7	14.34 ± 1.4	2.63	2.44 [1.73-5]	5.7
Bull shark (Carcharhinus leucas)	724 − 542 years cal.B.P.	4	-11.57 ± 0.90	15.22 ± 1.05	4.45	2.97 [0.38–8.52]	2.38

	Present	3	-11.73 ± 0.83	13.03 ± 0.85	2.13	1.06 [0.19–3.8]	0.58
Great white shark (Carcharodon carcharias)	724 − 542 years cal.B.P.	7	-11.71 ± 0.73	16.84 ± 0.59	1.19	0.99 [0.44–2.40]	1.54
	Present	1	-12.7	17.74	—	—	—
Tiger shark (Galeocerdo cuvier)	724 − 542 years cal.B.P.	7	-12.96 ± 1.44	14.10 ± 1.44	5.20	4.33 [2.03–10.40]	6.01
	Present	1	-13.50	11.91	—	—	—
Lemon shark (Negaprion brevirostris)	724 − 542 years cal.B.P.	4	-11.67 ± 1.21	15.52 ± 0.28	1.37	0.91 [0.26–2.82]	0.84

Average δ¹⁵N values ranged from 14.1‰ to 17.4‰ for the AC and 13.4‰ to 18.7‰ for the MC (Table 1). Similar patterns were observed for the most and least ¹⁵N-enriched in both communities. Among the apex predators in both communities, C. taurus, C. brachyurus and C. carcharias, had the most ¹⁵N-enriched δ¹⁵N values, whereas G. cuvier was the least ¹⁵N-enriched nitrogen isotopic values, also in both communities (Table 1).

C. taurus δ¹³C values among temporal communities did not significantly differ t = -0.25, p = 0.8.

Food web topology, isotopic niche variation and overlap

Isurus had the highest variability in SEAb the AC, whereas C. plumbeus had the highest variability in SEAb in the MC (Table 1). The highest SEAc area for the AC belongs to Isurus, and for the MC, belonging to C. plumbeus (Table 1). C. plumbeus have notably increase their isotopic niche (SEAc) in the present (from 1.67 to 7). An increase was also observed in the SEAc for C. taurus (SEAc from 2.35 to 2.8) and C. brachyurus (SEAc from 2.99 to 3.79). Other species decreased their SEAc from past to present, such as Isurus and C. leucas (Table 1).

Layman Metrics

In the MC, the higher C. taurus trophic position, along with lower δ15N values for Isurus and C. plumbeus resulted in a significantly larger NR value (prob = 0.99) (Fig. 3A). The MC had a significantly higher CD (prob = 0.99; Fig. 3A), denoting higher trophic diversity. When comparing to the MC, the AC species were tightly packaged within the isotopic space, suggesting higher trophic redundancy (lower NND, prob = 0.97; Fig. 3A).

Trophic position

The trophic position for C. taurus was significantly higher in the MC than the archaeological one (prob = 0.96; Fig. 3).

Our study demonstrated that even in samples dated hundreds of years old, SIA helps evaluate trophic and habitat assessment in multiple shark species using teeth collagen. Our assessment of the historical shark ecology showed three major differences between the archaeological and modern communities. First, the community of sharks off southern Brazil from 724 − 542 years cal.B.P were under a considerable degree of isotopic niche overlap, even when only considering the comparable species with the MC. On the other hand, the MC of sharks exhibited resource partitioning for C. taurus, mostly because of its higher trophic position (Fig. 4). Second, the MC had a higher CD, implying in a higher trophic diversity whereas the AC was characterized by species being close to each other, or 'packed', hence a higher trophic redundancy (e.g. species with similar diets and foraging methods; lower CD and NND respectively). Third, an increase in trophic position for C. taurus in the MC, could suggest a change in its role in its local ecosystem and could have important implications for other species in the local food web as well as for fisheries management. It is important to note that the isotopic functional evenness (NND and SDNND) and isotopic functional divergence (CD) indices are strongly robust to isotopic baseline shifts, which allows ecological inferences in the comparison of communities with different isotopic baselines (Belle and Cabana 2020).

Patterns of trophic structure

The classical niche theory predicts trophic segregation among coexisting species (Hutchinson 1957; Vandermeer 1972), and dietary niche partitioning in elasmobranch communities are regularly observed in community ecology studies (e.g. White et al. 2004; Kinney et al. 2011). However, we observed considerable isotopic niche overlap / trophic redundancy within the AC (Fig. 2). High niche overlap for a guild of sympatric predators would suggest that prey was not a limiting resource. Studies have shown high niche overlap and relaxed competition states between top consumers when food items are abundant, leading to stable resource use (e.g. Gallagher et al. 2016). Although pre-colonial environments in southern Brazil were likely to be resource-abundant, more factors would be at play in shaping the patterns of niche overlap observed. High niche overlap could also be the expected outcome of top-down controlled marine systems where predators are near their carrying capacity (Bas et al. 2019). Whereby when under higher states of competition, predators could experience frequent hunger effects, capturing prey according to their encounter rate (Gill 2003). This would lead the predators to share prey items with other competitors, hence sharing niche breadth (Bolnick et al. 2010). However, co-occurring archaeological shark species were not likely near carrying capacity, as these sharks too were under predation pressure from subsistence catches of pre-colonial natives (e.g. Fossile et al. 2019; Burg Mayer et al. 2022), and it is common for great sharks to predate smaller sharks (e.g. Smale 2005; Bornatowski et al. 2014). The sympatry of many apex consumers and the presence of intraguild predation would suggest the presence of a reinforced top-down control, even among the apex predators. Direct and indirect predation effects would also maintain predators and mesopredators populations below the carrying capacity that would be sustained by the abundance of prey resources (Heithaus 2008; Vaudo and Heithaus 2011). If this were the case in the AC, particular trophic levels of shark prey would be under predatory release, which would lead to higher degrees of trophic redundancy and niche overlap in the whole community (Heithaus 2008; Vaudo and Heithaus 2011).

Furthermore, food webs with multiple predators and intraguild predation often result in weakened interactions towards particular prey species (Schmitz 2007), whereas species-diverse food webs may offer prey populations greater resilience due to weaker or diffuse interactions (Montoya et al. 2006; Heithaus 2008), trophic redundancy, and populations of predators that are more resilient to decline (lower NND, Fig. 2; Heithaus 2008). The AC higher trophic redundancy would suggest these shark species were co-occurring, leading to a state of 'stable resource use'. In agreement with a higher degree of niche overlap, NND metric shows that species were more closely distributed in the AC (Fig. 2), suggesting higher trophic redundancy (Layman et al. 2007; Jabot et al. 2017).

Hence, we hypothesize that this multi-predator food web was able to sustain high levels of niche overlap through variable degrees of top-down control and intraguild predation, which would make several prey items under predatory release, leading the community to a state of 'stable resource use'.

Modern communities might be diversifying their patterns of resource use and decreasing their trophic redundancy, as other studies also have shown higher CD and NND for modern food webs (Saporiti et al. 2014; Bas et al. 2019). The niche hypothesis predicts that a population will exhibit a contracted niche breadth under the influence of strong interspecific competition and an expanded niche breadth when competition is relaxed, by the possibility of adding new resources that otherwise were monopolized by competitors (Bolnick et al. 2010). In previous historical trophic structure comparisons, decreases in niche overlap and trophic redundancy have been linked to competition release for top and mesopredators (Saporiti et al. 2014). Another explanation for the observed changes in the marine trophic ecology of the MC comes from the optimal foraging theory, which predicts that when prey becomes less abundant, predators become less selective increasing the consumption of less profitable prey and consequently increasing their trophic niche (Townsend and Winfield 1985; Gill 2003). As humans progress their unsustainable fisheries worldwide, fishing both top predators and their prey and impoverishing the food webs and their ecological relationships (Myers and Worm 2003; Pacoureau et al. 2021) it is plausible to assume that populations of top and mesopredators are progressively diversifying their diets. Both mechanisms cited might explain these observed changes, as in our study, all comparable species between past and present showed a shift towards depleted δ13C values and most of them had an increase in their isotopic niche (Fig. 2; Table 1), reinforcing the idea of a trend in niche and resource diversification. For example, the C. plumbeus deviance from expected enriched δ13C values for typical coastal species, likewise for some individuals of C. taurus (Fig. 2), would suggest that the relative importance of pelagic prey has increased. Changes in isotopic baselines may hinder isotopic comparisons between time-separated communities, but we suggest that based on C. taurus δ13C values among temporal communities that did not significantly differ, the baseline for coastal areas has remained relatively similar.

Regardless, the increase in the trophic niche for these species symbolizes the plasticity of sharks to alter their trophic ecology, a feature that must be attributed to their long evolutionary history that has enabled them to adapt to different environmental conditions and prey availability. This plasticity may also have implications for their resilience to human impacts and their role in marine ecosystems.

The increased trophic position of modern Carcharias taurus

Marine food webs often contain four or five trophic levels (Vander-Zanden and Fetzer 2007), and the increase in trophic position generally means that more predation events are taking place. Previous trophic reconstructions studies from archaeological datasets in South America suggested that intensively exploited modern fur seals and sea lions increased their trophic level as a consequence of liberation from intraspecific competition (Drago et al. 2009; Saporiti et al. 2014; Zenteno et al. 2015; Bas et al. 2019). A similar situation could be playing a role in niche partitioning and the increased trophic position of C. taurus, as this species is considered to be overexploited or threatened with overexploitation (ICMBio 2018). The proposed mechanism behind the increase in trophic level involves a niche shift towards a more selective diet on bigger prey as a consequence of intraspecific competition release (Saporiti et al. 2014; Bas et al. 2019), hence a higher trophic level (Jennings 2005). C. taurus is mainly a predator of intermediate and higher trophic level elasmobranchs and teleosts (Lucifora et al. 2009; Cortés 1999; Hussey et al. 2015), and competition release may have benefited C. taurus, enabling the increase in high trophic level prey in its diet. The intraspecific competition release in question should be even more dramatic for elasmobranchs, as they have lower population replenishment after severe exploitation, due to their intrinsic life-history traits, such as late maturity, slow growth and low reproductive rates (Ferretti et al. 2010). Furthermore, populations of marine predators, under fishing pressure would have constrained growth rates, due to direct and indirect effects of predation (Heithaus 2008). Lower population growth rates would indirectly reduce trophic levels, as it correlates with body size (Jennings 2005), which does not seem to be the case for C. taurus in this study.

Modern specimens of C. taurus and Carcharhinus group have expanded their niche areas in the present (respectively: SEAc from 2.35 to 2.8; and SEAc from 1.6 to 7). As mentioned before, the niche hypothesis might explain this increase in the isotopic niche, suggesting relaxed competition states, thus corroborating the hypothesis that intraspecific competition release is causing the observed increase in trophic level for C. taurus, and maybe other Carcharhinidae.

In addition, there is mounting evidence that anthropic impacts cause longer food webs (longer NR; Fig. 3) through hunting and fisheries, leading to intraspecific competition release for some species (Drago et al. 2009; Saporiti et al. 2014; Zenteno et al. 2015; Bas et al. 2019).

Caveats and considerations

It may not be surprising that two isotopic snapshots of shark guilds varied over time, reflecting changes in their underlying ecological dynamics. However, in this study, we aimed to describe and report shifts in their trophic structure/topology. It is important to note that these changes in topology are not influenced by isotopic baselines, providing evidence for changes driven by shifts in the species interactions, by anthropic impacts within these systems or the synergy of both. This raises important questions for future research, such as whether similar patterns of variation can be observed in other studies, and what the potential drivers of these changes might be. While we cannot definitively attribute the observed differences in food web topology to anthropogenic impacts, it is likely that human activities have played a role in altering the trophic positions of C. taurus and possibly other species. Further investigation using historical data will be necessary to understand the causes and consequences of these changes.

We understand our study is not free of many caveats that comes from using stable isotopes inferences (Hussey et al. 2012b; Shiffman et al. 2012). Turnover rates for teeth only provide inferred average resource use, thus the pattern of niche overlap for AC could be representative of temporal niche partitioning over the same resources. When there are numerous different pathways between baseline primary producers or secondary consumers and the target organisms under research, the evaluation of niche can become problematic for some highly migratory shark species that feed in multiple habitats (e.g. C. carcharias, C. obscurus). When dealing with isotopic niche areas, absence of overlap may provide evidence for resource partitioning, however the presence of overlap may not always mean shared sources use, as different patterns of resource use may lead to similar isotopic values (reviewed in Layman et al. 2012). However, we could assume that species are sympatric and therefore did share resources, based in other pre-colonial inhabitants of Brazil, the pre-colonial people mostly likely did not performed extreme far-away fishing trips away from the coast (Gilson and Lessa 2019) even catching typically oceanic species near the coast, as shown for I. paucus individuals with enriched carbon values (Fig. 2). Furthermore, high niche overlap among sharks may not be an uncommon occurrence (e.g. Vaudo and Heithaus 2011; Gallagher et al. 2016; Shiffman et al. 2019), although other ecological dynamics may be involved in these examples, this corroborates the plausibility of our findings.

The calculation of a trophic level using a single discrimination factor obscures much of the real complexity behind trophic interactions (Zeichner et al. 2017), whereas scaled discrimination factors may be more accurate (Hussey et al. 2014). It is difficult to speculate on the nature of high rates of niche overlap without further knowledge about past food webs, trophic interactions for rare species, and respective regional past isoescapes. The lack of studies using stable isotopes in sharks in Brazil and available data on regional isoescapes also hampers any comparative studies.

Concluding remarks

Our study adds to the multiple trophic reconstructions of food webs that have found patterns of tightly ‘packed’ communities (NND) in pre-colonial food webs, and patterns of increased trophic diversity (CD) for modern communities and increased trophic position for some species (e.g. Saporiti et al. 2014; Bas et al. 2019; Durante et al. 2022). This would suggest a possible pattern for the use of resource in nearly pristine food webs, where trophic redundancy is common. The increase in the trophic position of apex predators and the increase in the diversity of resource use in modern communities needs attention. There is concern that the simplification of ecosystems, due to the loss of species and ecological interactions, leads to diminished functional redundancy and lower ecosystem resistance and resilience (Worm et al. 2006; Bascompte et al. 2005).

This study shows a possible consequence of anthropic actions that affect trophic interactions and ecology of surviving individuals of populations that would be below carrying capacity, as most sharks populations are sensitive to fishing mortality (Dulvy and Forrest 2010; Ferretti et al. 2010). Until further action is taken to prevent the disappearance of many important species, food webs are becoming gradually poorer than they were before.

ACKNOWLEDGEMENTS

We would like to thank the National Geographic Society (#EC-400R-18) for the funding that was vital to this study. To CAPES for the master's degree scholarship. To the post-graduate ecology program (PPGECO-UFSC). To Jules M.R. Soto and Bibiana C. Lessa from the Univali Oceanographic Museum (MOVI), for welcoming us into the Museum's space and providing samples that were essential for this study. To Simon-Pierre Gilson and Luciane Scherer, for welcoming us to the research center of the Museum of Archeology and Ethnology at UFSC. We thank Karla Scherer for welcoming her into her workspace and helping on countless occasions. We would also like to thank the UFSC multi-user laboratory, LAMEB. Finally, we would like to thank Clarissa Teixeira and Luiza Pereira for their guidance in the world of stable isotopes.

Funding (information that explains whether and by whom the research was supported)

This research was funded through National Geographic Society, early career grant, of number EC-400R-18.

Conflicts of interest/Competing interests (include appropriate disclosures)

The author informs that no conflict of interest is present.

Ethics approval (include appropriate approvals or waivers)

Ethics approval was not required for this study according to local legislation [11.794 (Arouca Law) / October 8 2008]. Approval to the use of archaeological material in research was obtained through protocol 01500.900346/2017-98 of IPHAN (INSTITUTE OF NATIONAL HISTORIC AND ARTISTIC HERITAGE [‘INSTITUTO DO PATRIMÔNIO HISTÓRICO E ARTÍSTICO NACIONAL’]).

Consent to participate (include appropriate statements)

Does not apply

Consent for publication (include appropriate statements)

Does not apply

Availability of data and material (data transparency)

The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

Code availability (software application or custom code)

Does not apply

Authors' contributions

GBM conceived the study and designed the experiments. Material preparation and data collection were performed by all authors. Data analysis was performed by GBM. The first draft of the manuscript was written by GBM and RHAF revised and commented on previous versions of the manuscript. All authors helped with funding acquisition. All authors read and approved the final manuscript.

Barreto RR, Ferretti F, Flemming JM, Amorim A, Andrade H, Worm B, Lessa R (2016) Trends in the exploitation of South Atlantic shark populations. Conservation Biology 30:792–804. https://doi.org/10.1111/cobi.12663
Bas M, Briz I Godino I, Álvarez M, Vales DG, Crespo EA, Cardona L (2019) Back to the future? Late Holocene marine food web structure in a warm climatic phase as a predictor of trophodynamics in a warmer South‐Western Atlantic Ocean. Global Change Biology 2:404-419. https://doi.org/10.1111/gcb.14523
Baum JK, Worm B (2009) Cascading top-down effects of changing oceanic predator abundances. Journal of Animal Ecology 78:699–714. https://doi.org/10.1111/j.1365-2656.2009.01531.x
Belle S, Cabana G (2020) Effects of changes in isotopic baselines on the evaluation of food web structure using isotopic functional indices. PeerJ. doi: 10.7717/peerj.9999
Bolnick DI, Ingram T, Stutz WE, Snowber LK, Lau OL, Paull JS (2010) Ecological release from interspecific competition leads to decoupled changes in population and individual niche width. Proceedings of the Royal Society B: Biological Sciences 277:1789–1797. https://doi.org/10.1098/rspb.2010.0018
Bornatowski H, Braga RR, Abilhoa V, Corrêa MFM (2014) Feeding ecology and trophic comparisons of six shark species in a coastal ecosystem off southern Brazil. Journal of Fish Biology 85:246–263. https://doi.org/10.1111/jfb.12417
Burg Mayer G, de Souza ECS, Gilson S-P, Freitas RHA (2022) South Brazil pre-colonial sharks: Insights into biodiversity and species distributions. Journal of Fish Biology 100(3):811– 819. https://doi.org/10.1111/jfb.14998
Caut S, Angulo E, Courchamp F (2009) Variation in discrimination factors (Δ15N and Δ13C): the effect of diet isotopic values and applications for diet reconstruction. Journal of Applied Ecology 46:443–453. https://doi.org/10.1111/j.1365-2664.2009.01620.x
Chiessi CM, Mulitza S, Groeneveld J, Silva JB, Campos MC, Gurgel MHC (2014) Variability of the Brazil Current during the late Holocene. Palaeogeography, Palaeoclimatology, Palaeoecology 415:28–36. https://doi.org/10.1016/j.palaeo.2013.12.005
Cortés (1999) Standardized diet compositions and trophic levels of sharks. ICES Journal of Marine Science 56:707–717. https://doi.org/10.1006/jmsc.1999.0489
DeNiro MJ (1985) Postmortem preservation and alteration of in vivo bone collagen isotope ratios in relation to palaeodietary reconstruction. Nature 317:806–809. https://doi.org/10.1038/317806a0
Dicken ML, Hussey NE, Christiansen HM, Smale MJ, Nkabi N, Cliff G, Wintner SP (2017) Diet and trophic ecology of the tiger shark (Galeocerdo cuvier) from South African waters. PLOS ONE 12:e0177897 doi: 10.1371/journal.pone.0177897
Dobberstein RC, Collins MJ, Craig OE, Taylor G, Penkman KEH, Ritz-Timme S (2009) Archaeological collagen: Why worry about collagen diagenesis? Archaeological and Anthropological Sciences 1:31–42. https://doi.org/10.1007/s12520-009-0002-7
Doney SC, Ruckelshaus M, Duffy EJ, Barry JP, Chan F, English CA, Talley LD (2012) Climate Change Impacts on Marine Ecosystems. Annual Review of Marine Science 4(1):11–37. https://doi.org/10.1146/annurev-marine-041911-111611
Drago M, Cardona L, Franco-Trecu V, Crespo EA, Vales DG, Borella F, Zenteno L, Gonzáles EM, Inchausti P (2017) Isotopic niche partitioning between two apex predators over time. Journal of Animal Ecology 86:766–780. https://doi.org/10.1111/1365-2656.12666
‌Drago M, Crespo E, Aguilar A, Cardona L, Garcia N, Dans SL, Goodall N (2009) Historic diet change of the South American sea lion in Patagonia as revealed by isotopic analysis. Marine Ecology Progress Series 384:273–286. https://doi.org/10.3354/meps08017
Dulvy NK, Pacoureau N, Rigby CL, et al (2021) Overfishing drives over one-third of all sharks and rays toward a global extinction crisis. Curr Biol 31:4773-4787.e8. https://doi.org/10.1016/j.cub.2021.08.062
Dulvy NK, Forrest RE (2010) Life Histories, Population Dynamics, and Extinction Risks in Chondrichthyans. Taylor & Francis 655–696. https://doi.org/10.1201/9781420080483-24
Durante L, Wing S, Ingram T, Sabadel A, Shima J (2022) Changes in trophic structure of an exploited fish community at the centennial scale are linked to fisheries and climate forces. Scientific Reports 12:1–12. doi: 10.1038/s41598-022-08391-x
‌Ebert DA, Fowler SL, Compagno LJ (2013) Sharks of the world: a fully illustrated guide. Wild Nature Press.
Enax J, Prymak O, Raabe D, Epple M (2012) Structure, composition, and mechanical properties of shark teeth. Journal of Structural Biology 178:290–299. https://doi.org/10.1016/j.jsb.2012.03.012
Erlandson JM, Rick TC (2008) Human Impacts on Ancient Marine Ecosystems, 1^st ed. University of California Press, Los Angeles California USA.
Estrada JA, Rice AN, Natanson LJ, Skomal GB (2006) Use of isotopic analysis of vertebrae in reconstructing ontogenetic feeding ecology in white sharks. Ecology 87:829–834. https://doi.org/10.1890/0012-9658(2006)87[829:uoiaov]2.0.co;2
Ferretti F, Worm B, Britten GL, Heithaus MR, Lotze HK (2010) Patterns and ecosystem consequences of shark declines in the ocean. Ecology Letters 13:1055-1071. https://doi.org/10.1111/j.1461-0248.2010.01489.x
Fossari TD (2004) A população pré-colonial Jê na paisagem da Ilha de Santa Catarina. PhD Thesis, Universidade Federal de Santa Catarina, Florianópolis, Brazil.
Fossile T, Ferreira J, da Rocha Bandeira D, et al (2019) Pre-Columbian fisheries catch reconstruction for a subtropical estuary in South America. Fish and Fisheries 20(6):1124–1137. https://doi.org/10.1111/faf.12401
France R (1995) Carbon-13 enrichment in benthic compared to planktonic algae: foodweb implications. Marine Ecology Progress Series 124:307–312. https://doi.org/10.3354/meps124307
France R, Peters R (1997) Ecosystem differences in the trophic enrichment of ¹³C in aquatic food webs. Canadian Journal of Fisheries and Aquatic Sciences 54:1255–1258. https://doi.org/10.1139/f97-044
Froese R, Pauly D (2018) FishBase: worldwide web electronic publication. https://fishbase.org/. Accessed 02 August 2022
Gallagher AJ, Shiffman DS, Byrnes EE, Hammerschlag-Peyer CM, Hammerschlag N (2017) Patterns of resource use and isotopic niche overlap among three species of sharks occurring within a protected subtropical estuary. Aquatic Ecology 51:435–448. https://doi.org/10.1007/s10452-017-9627-2
Gill AB (2003) The dynamics of prey choice in fish: the importance of prey size and satiation. Journal of Fish Biology 63:105–116. https://doi.org/10.1111/j.1095-8649.2003.00214.x
Gilson SP, Lessa A (2019) Human-Sharks interaction in chroniclers’ accounts from the XVIth and XVIIth centuries: A rich source of information for Brazilian zooarchaeological studies. Archaeofauna 28:157–167. 10.15366/archaeofauna2019.28.013
Hammerschlag N, Williams L, Fallows M, Fallows C (2019) Disappearance of white sharks leads to the novel emergence of an allopatric apex predator, the sevengill shark. Sci Rep 9(1):1-6. https://doi.org/10.1038/s41598-018-37576-6
Heithaus MR, Frid A, Wirsing AJ, Worm B (2008) Predicting ecological consequences of marine top predator declines. Trends in Ecology & Evolution 23:202–210. https://doi.org/10.1016/j.tree.2008.01.003
Heileman S, Gasalla M (2009) XVI-54 South Brazil Shelf: LME# 15. The UNEP Ecosystem Report: a perspective on changing conditions in LMEs of the World’s Regional Seas. UNEP Regional Seas Report and Studies 182:723-734.
Hobson KA (1999) Tracing origins and migration of wildlife using stable isotopes: a review. Oecologia 120:314–326. https://doi.org/10.1007/s004420050865
Hussey NE, MacNeil MA, McMeans BC, Olin JA, Dudley SFJ, Cliff G, Wintner SP, Fennessy ST, Fisk AT (2014) Rescaling the trophic structure of marine food webs. Ecology Letters 17:239–250. https://doi.org/10.1111/ele.12226
‌Hussey NE, MacNeil MA, Olin JA, McMeans BC, Kinney MJ, Chapman DD, Fisk AT (2012b) Stable isotopes and elasmobranchs: tissue types, methods, applications and assumptions. Journal of Fish Biology 80:1449–1484. https://doi.org/10.1111/j.1095-8649.2012.03251.x
‌Hussey NE, MacNeil MA, Siple MC, Popp, BN, Dudley SFJ, Fisk AT (2015) Expanded trophic complexity among large sharks. Food Webs 4:1–7. https://doi.org/10.1016/j.fooweb.2015.04.002
Hussey NE, McCann HM, Cliff G, Dudley SF, Wintner SP, Fisk AT (2012a) Size-Based Analysis of Diet and Trophic Position of the White Shark, Carcharodon carcharias, in South African Waters. Global Perspectives on the Biology and Life History of the White Shark 27–50. https://doi.org/10.1201/b11532-5
‌Hutchinson, EG (1957) Concluding Remarks. Population Studies: Animal Ecology and Demography. Cold Springs Harbor Symposia on Quantitative Biology 22:415-27.
ICMBio Instituto Chico Mendes de Conservação da Biodiversidade (2018) Livro vermelho da fauna brasileira ameaçada de extinção. VI–Peixes.
Indermühle A, Stocker TF, Joos F, Fischer H, Smith HJ, Wahler M, Deck B, Mastroianni D, Tschumi J, Blunier T, Meyer R, Stauffer B (1999) Holocene carbon-cycle dynamics based on CO2 trapped in ice at Taylor Dome, Antarctica. Nature 398:121–126. https://doi.org/10.1038/18158
Jackson AL, Inger R, Parnell AC, Bearhop S (2011) Comparing isotopic niche widths among and within communities: SIBER – Stable Isotope Bayesian Ellipses in R. Journal of Animal Ecology 80:595–602. https://doi.org/10.1111/j.1365-2656.2011.01806.x
Jackson JB, Kirby MX, Berger WH, Bjorndal KA, Botsford LW, Bourque BJ, Bradbury RH, Cooke R, Erlandson J, Estes JA, Hughes TP, Kidwell S, Lange CB, Lenihan HS, Pandolfi JM, Peterson CH, Steneck RS, Tegner MJ, Warner RR (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629–37. https://doi.org/10.1126/science.1059199
Jennings S (2005) Size-based analyses of aquatic food webs. Aquatic food webs: an ecosystem approach. Oxford University Press, Oxford, 86-97.
Kemp NE (1984) Organic Matrices and Mineral Crystallites in Vertebrate Scales, Teeth and Skeletons. American Zoologist 24:965–976. https://doi.org/10.1093/icb/24.4.965
Kim SL, Koch PL (2012) Methods to collect, preserve, and prepare elasmobranch tissues for stable isotope analysis. Environmental Biology of Fishes 95:53–63. https://doi.org/10.1007/s10641-011-9860-9
Kinney MJ, Hussey NE, Fisk AT, Tobin AJ, Simpfendorfer CA (2011) Communal or competitive? Stable isotope analysis provides evidence of resource partitioning within a communal shark nursery. Marine Ecology Progress Series 439:263–276. https://doi.org/10.3354/meps09327
Kotas JE (2005) A pesca de emalhe e de espinhel-de-superfície na Região Sudeste-Sul do Brasil. Instituto Oceanográﬁco-USP.
Layman CA, Araujo MS, Boucek R, Hammerschalg-Peyer CM, Harrison E, Jud ZR, Matich P, Rosenblatt AE, Vaudo JJ, Yeager LA, Post DM, Bearhop S (2012) Applying stable isotopes to examine food-web structure: an overview of analytical tools. Biological Reviews 87:545–562. https://doi.org/10.1111/j.1469-185x.2011.00208.x
Layman CA, Arrington DA, Montaña CG, Post DM (2007) Can stable isotope ratios provide for community-wide measures of trophic structure?. Ecology 88:42–48. https://doi.org/10.1890/0012-9658(2007)88[42:csirpf]2.0.co;2
LeGeros, R.Z. (1981) Apatites in Biological Systems. Progress in Crystal Growth and Characterization of Materials, 4:1-45. https://doi.org/10.1016/0146-3535(81)90046-0.
Lopes MS, Bertucci TCP, Rapagnã L, Tubin, RA, Monteiro-Neto C, Tomas ARG, Tenório MC, Lima T, Souza R, Carrillo-Briceño JD, Haimovici M, Macario K, Carvalho C, Aguilera Socorro O (2016) The Path towards Endangered Species: Prehistoric Fisheries in Southeastern Brazil. PLOS ONE 11:e0154476. https://doi.org/10.1371/journal.pone.0154476
‌Lübke A, Enax J, Loza K, Prymak O, Gaengler P, Fabritius HO, Raabe D,
Epple M (2015) Dental lessons from past to present: ultrastructure and composition of teeth from plesiosaurs, dinosaurs, extinct and recent sharks. RSC Advances 5:61612–61622. https://doi.org/10.1039/c5ra11560d
Lucifora LO, García VB, Escalante AH (2009) How can the feeding habits of the sand tiger shark influence the success of conservation programs? Animal Conservation 12:291–301. https://doi.org/10.1111/j.1469-1795.2009.00247.x
Mahiques MM, Coaracy Wainer IK, Burone L, Nagai R, Mello e Souza SH, Figueira RCL, Silveira ICA, Bícego MC, Alves DPV, Hammer Ø (2009) A high-resolution Holocene record on the Southern Brazilian shelf: Paleoenvironmental implications. Quaternary International 206:52–61. https://doi.org/10.1016/j.quaint.2008.09.010
Mahiques MM, Sousa SH de M, Furtado VV, Tessler MG, Toledo FAL, Burone L, Figueira RCL, Klein DA, Martins CC, Alves DPV (2010) The Southern Brazilian shelf: general characteristics, quaternary evolution and sediment distribution. Brazilian Journal of Oceanography 58:25–34. https://doi.org/10.1590/s1679-87592010000600004
Maureaud A, Gascuel D, Colléter M, Palomares MLD, Pontavice HD, Pauly D, Cheung WWL (2017) Global change in the trophic functioning of marine food webs. PLOS ONE 12:e0182826. https://doi.org/10.1371/journal.pone.0182826
Mendes AB, Duarte MR, Silva EP (2018) Biodiversity of Holocene marine fish of the southeast coast of Brazil. Biota Neotropica 18(1): e20170394. http://dx.doi.org/10.1590/1676-0611-BN-2017-0394
Milessi AC, Arancibia H, Neira S, Defeo O (2005) The mean trophic level of Uruguayan landings during the period 1990–2001. Fisheries Research 74:223–231. https://doi.org/10.1016/j.fishres.2005.02.002
Montoya JM, Pimm SL, Solé RV (2006) Ecological networks and their fragility. Nature 442(7100):259–264. https://doi.org/10.1038_nature04927.
Myers RA, Baum JK, Shepherd TD, Powers SP, Peterson CH (2007) Cascading Effects of the Loss of Apex Predatory Sharks from a Coastal Ocean. Science 315:1846–1850. https://doi.org/10.1126/science.1138657
‌Myers RA, Worm B (2003) Rapid worldwide depletion of predatory fish communities. Nature 423:280–283. https://doi.org/10.1038/nature01610
Nagai RH, Sousa SHM, Mahiques MM (2014) Chapter 5 The southern Brazilian shelf. Geological Society, London, Memoirs 41:47–54. https://doi.org/10.1144/m41.5
Newsome SD, Clementz MT, Koch PL (2010) Using stable isotope biogeochemistry to study marine mammal ecology. Marine Mammal Science. https://doi.org/10.1111/j.1748-7692.2009.00354.x
Pacoureau N, Rigby CL, Kyne PM, Sherley RB, Winker H, Carlson JK, Fordham S V., Barreto RP, Fernando D, Francis MP, Jabado RW, Herman KB, Liu K-M, Marshall AD, Pollom RA, Romanov E V., Simpfendorfer CA, Yin JS, Kindsvater HK, Dulvy NK (2021) Half a century of global decline in oceanic sharks and rays. Nature Rev. doi: 10.1038/s41586-020-03173-9
Pauly D, Christensen V, Dalsgaard J, et al (1998) Fishing down marine food webs. Science 279:860–863. https://doi.org/10.1126/science.279.5352.860
Parnell A, Jackson A (2013). Siar: Stable Isotope Analysis in R. R package version 4.2.
Pereira MD, Schettini CAF, Omachi CY (2009) Caracterização de feições oceanográficas na plataforma de Santa Catarina através de imagens orbitais. Revista Brasileira de Geofísica 27:81-93. https://doi.org/10.1590/s0102-261x2009000100007
Piola AR, Campos EJD, Möller OO, et al (2000) Subtropical Shelf Front off eastern South America. Journal of Geophysical Research: Oceans 105:6565–6578. https://doi.org/10.1029/1999jc000300
Quezada-Romegialli C, Jackson AL, Hayden B, Kahilainen KK, Lopes C, Harrod C (2018) tRophicPosition, an r package for the Bayesian estimation of trophic position from consumer stable isotope ratios. Methods in Ecology and Evolution 9:1592–1599. https://doi.org/10.1111/2041-210x.13009
R Core Team (2018). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
Reitz E, Wing E (2008) Zooarchaeology. 2ª ed. Cambridge University Press. Cambridge, England.
Roff G, Doropoulos C, Rogers A, Bozec YM, Krueck NC, Aurellado E, Priest M, Birrell C, Mumby PJ. (2016) The Ecological Role of Sharks on Coral Reefs. Trends in Ecology & Evolution 31:395–407. https://doi.org/10.1016/j.tree.2016.02.014
Santos MC, Faria-Junior E, Freitas RHA (2020) Reconhecimento etnoecológico sobre o tubarão-mangona Carcharias taurus sob a perspectiva de pescadores artesanais da grande Florianópolis-SC, Brasil. Rev Nord Biol 27(1):143-157. https://doi.org/10.22478/ufpb.2236-1480.2019v27n1.47526
Saporiti F, Bearhop S, Silva L, Vales DG, Zenteno L, Crespo EA, Aguilar A, Cardona L (2014) Longer and Less Overlapping Food Webs in Anthropically Disturbed Marine Ecosystems: Confirmations from the Past. PloS ONE 9:e103132. https://doi.org/10.1371/journal.pone.0103132
Schmitz OJ (2007) Predator diversity and trophic interactions. Ecology 88:2415–2426. https://doi.org/10.1890/06-0937.1
‌Shiffman DS, Gallagher AJ, Boyle MD, Hammerschlag-Peyer CM, Hammerschlag N (2012) Stable isotope analysis as a tool for elasmobranch conservation research: a primer for non-specialists. Marine and Freshwater Research 63:635. https://doi.org/10.1071/mf11235
Shiffman DS, Kaufman L, Heithaus M, Hammerschlag N (2019) Intraspecific differences in relative isotopic niche area and overlap of co-occurring sharks. Aquatic Ecology 1-18. https://doi.org/10.1007/s10452-019-09685-5
‌Shimada K (2003) The relationship between the tooth size and total body length in the white shark, Carcharodon carcharias (Lamniformes: Lamnidae). Journal of Fossil Research 35:28–33.
Shimada K (2004) The relationship between the tooth size and total body length in the sandtiger shark, Carcharias taurus (Lamniformes : Odontaspididae). Journal of fossil research. 37:76-81.
Smale MJ (2005) The diet of the ragged-tooth shark Carcharias taurus Rafinesque 1810 in the Eastern Cape, South Africa. In: African Journal of Marine Science. 27:331-335. https://doi.org/10.2989/18142320509504091
Szpak P (2011) Fish bone chemistry and ultrastructure: implications for taphonomy and stable isotope analysis. Journal of Archaeological Science 38:3358–3372. https://doi.org/10.1016/j.jas.2011.07.022
Townsend CR, Winfield IJ (1985). The application of optimal foraging theory to feeding behavior. In: Tytler P, Calow P (eds) Fish energetics: new perspectives. John Hopkins University Press, Baltimore, pp 67–98. https://doi.org/10.1007/978-94-011-7918-8
Tuross N, Fogel ML, Hare P (1988) Variability in the preservation of the isotopic composition of collagen from fossil bone. Geochimica et Cosmochimica Acta 52:929–935. https://doi.org/10.1016/0016-7037(88)90364-x
Vales DG, Cardona L, Zangrando AF, Borella F, Saporiti F, Goodall RN, de Oliveira LR, Crespo EA (2017) Holocene changes in the trophic ecology of an apex marine predator in the South Atlantic Ocean. Oecologia 183:555–570. https://doi.org/10.1007/s00442-016-3781-4
Vandermeer, JH (1972) Niche theory. Annual Review of Ecology and Systematics 3:107-132. https://doi.org/10.1146/annurev.es.03.110172.000543
Vander-Zanden JM, Fetzer WW (2007) Global patterns of aquatic food chain length. Oikos 116:1378–1388. https://doi.org/10.1111/j.0030-1299.2007.16036.x
Vaudo J, Heithaus M (2011) Dietary niche overlap in a nearshore elasmobranch mesopredator community. Marine Ecology Progress Series 425:247–260. https://doi.org/10.3354/meps08988
Vennemann T., Hegner E, Cliff G, Benz G. (2001) Isotopic composition of recent shark teeth as a proxy for environmental conditions. Geochimica et Cosmochimica Acta 65:1583–1599. https://doi.org/10.1016/s0016-7037(00)00629-3
White WT, Platell ME, Potter IC (2004) Comparisons between the diets of four abundant species of elasmobranchs in a subtropical embayment: implications for resource partitioning. Marine Biology 144:439–448. https://doi.org/10.1007/s00227-003-1218-1
Worm B, Barbier EB, Beaumont N, Duffy JE, Folke C, Halpern BS, Jackson JBC, Lotze HK, Michelli F, Palumbi SR, Selkoe KA, Stachowicz JJ, Watson R (2006) Impacts of Biodiversity Loss on Ocean Ecosystem Services. Science 314:787–790. https://doi.org/10.1126/science.1132294
Worm B, Davis B, Kettemer L, Ward-Paige CA, Chapman Demian, Heithaus MR, Kessel ST, Gruber SH (2013) Global catches, exploitation rates, and rebuilding options for sharks. Marine Policy 40:194–204. https://doi.org/10.1016/j.marpol.2012.12.034
Vooren CM, Klippel S (2005) Ações para a conservação de tubarões e raias no sul do Brasil. Igaré, Porto Alegre.
Zeichner SS, Colman AS, Koch PL, Polo-Silva C, Galván-Magaña F, Kim SL (2017) Discrimination Factors and Incorporation Rates for Organic Matrix in Shark Teeth Based on a Captive Feeding Study. Physiological and biochemical zoology 90:257–272. https://doi.org/10.1086/689192
Zenteno L, Crespo E, Vales D, Silva L, Saporiti F, Oliveira LR, Secchi R, Drago M, Aguilar A, Cardona L (2015) Dietary consistency of male South American sea lions (Otaria flavescens) in southern Brazil during three decades inferred from stable isotope analysis. Marine Biology 162:275–289. https://doi.org/10.1007/s00227-014-2597-1

Download PDF

Journal Publication

published 05 Jul, 2023

Read the published version in Marine Biology →

Editorial decision: Revise and Resubmit
05 Apr, 2023
Reviewers agreed at journal
24 Mar, 2023
Editor assigned by journal
24 Mar, 2023
First submitted to journal
21 Mar, 2023

You are reading this latest preprint version

Archaeological sharks: Late Holocene changes in trophic ecology and habitat use of sharks in South Brazil

Status:

Journal Publication

Version 1

Abstract

Figures

Introduction

Materials And Methods

Study area and sampling

Sample preparation and methodological adaptations

Data Analysis

Results

Variation in C:N ratios and δ¹³C - δ¹⁵N

Food web topology, isotopic niche variation and overlap

Layman Metrics

Trophic position

Discussion

Patterns of trophic structure

The increased trophic position of modern Carcharias taurus

Caveats and considerations

Concluding remarks

Declarations

Funding (information that explains whether and by whom the research was supported)

References

Supplementary Files

Status:

Journal Publication

Version 1

Archaeological sharks: Late Holocene changes in trophic ecology and habitat use of sharks in South Brazil

Status:

Journal Publication

Version 1

Abstract

Figures

Introduction

Materials And Methods

Study area and sampling

Sample preparation and methodological adaptations

Data Analysis

Results

Variation in C:N ratios and δ13C - δ15N

Food web topology, isotopic niche variation and overlap

Layman Metrics

Trophic position

Discussion

Patterns of trophic structure

The increased trophic position of modern Carcharias taurus

Caveats and considerations

Concluding remarks

Declarations

Funding (information that explains whether and by whom the research was supported)

References

Supplementary Files

Status:

Journal Publication

Version 1

Variation in C:N ratios and δ¹³C - δ¹⁵N