Environ Biol Fish (2009) 84:41–52 DOI 10.1007/s10641-008-9387-x

Changes in trophic level of Squatina guggenheim with increasing body length: relationships with type, size and trophic level of its prey Rodolfo Vögler & Andrés C. Milessi & Luis O. Duarte Received: 9 April 2007 / Accepted: 24 July 2008 / Published online: 27 August 2008 # Springer Science + Business Media B.V. 2008

Abstract The occurrence of changes in the trophic level (TL) of sharks with growth has not been quantified until now. Here length-related changes on Squatina guggenheim Marini trophic level were determined, and shifts in type, size and trophic level of its prey were analysed. Sampling took place during five bottom trawl surveys conducted in the Argentine– Uruguayan Common Fishing Zone during spring (December/1995, October/1997) and fall (March/ 1997, March–April/1998, May–June/1998), using an Engel bottom-trawl net to capture the sharks. Three length groups were defined based on diet composition and using a cluster analysis (group I, 23–60 cm; group II, 61–80 cm; group III, 81–91 cm LT). An ANOSIM procedure detected significant differences (P<0.05) in the diet spectrum between the three length groups. The R. Vögler (*) Programa de Doctorado, Centro Interdisciplinario de Ciencias Marinas, Av. Instituto Politécnico Nacional s/n. Col. Playa Palo de Santa Rita, CP 952 La Paz, Baja California Sur, México e-mail: [email protected] A. C. Milessi Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Rivadavia 1917, Buenos Aires, Argentina L. O. Duarte Laboratorio de Investigaciones Pesqueras Tropicales, Universidad del Magdalena, Cra. 32 # 22-08, Santa Marta, Colombia

smallest sharks (group I) ingested fish prey ranging from 5 to 21 cm LT, medium sharks (group II) fed on fish prey between 11 and 35 cm LT, and largest sharks (group III) preyed on fish between 13 and 40 cm LT. Diet structure of length groups were discriminated by almost the same prey taxa that characterized them. The increase of S. guggenheim body length promoted a decrease in the relative importance of small pelagic fishes. Contrarily, prey as medium benthopelagic fishes, medium pelagic squid and medium benthopelagic fishes showed an inverse tendency, indicating a broad diet spectrum of adults. Predator-length and prey-length relationship indicated a trend where 44.8% of S. guggenheim diet was integrated by prey <20% of their own body length and 32.8% of their diet was composed by prey >30% of their own length. The increase of mean prey weight was associated with the increase of predator weight and length. Smallest sharks (group I) were identified as secondary consumers (TL<4) whereas medium sharks (group II) and largest sharks (group III) were placed as tertiary consumers (TL>4). The study revealed an increase in S. guggenheim TL with shark growth as a consequence of changes on type, size and TL of prey ingested. Keywords Angular angel shark . Feeding ecology . Predator–prey interactions . Uruguay . Marine food webs

Introduction Sharks are typical top predators in marine ecosystems (Stevens et al. 2000), playing a major role in the

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energy fluxes exchange between upper and lower trophic levels (Wetherbee and Cortés 2004). In spite of growing interest in shark feeding ecology over the last decade (e.g. Brewer et al. 1995; Cortés et al. 1996; Ellis et al. 1996; White et al. 2004), the first study that estimated the position of 149 shark species in marine food webs (Cortés 1999) was accomplished only recently. Numerous studies have found that both type and size of prey ingested change with increasing predator size (Lyle 1983; Werner and Gilliam 1984; Platell et al. 1998; Schefer et al. 2002; Cherel and Duhamel 2004; Wetherbee and Cortés 2004). However, diet shifts are more often reported qualitatively rather than based on rigorous statistical analysis. Squatina guggenheim is one of the most widespread endemic elasmobranchs inhabiting bottom waters of the Southwest Atlantic (33°–41° S) coastal ecosystem (Vögler et al. 2008). This bottom-dwelling shark is an important fishing resource caught off the coastal zones of Uruguay (Paesch and Meneses 1999), southern Brazil (Villwock and Vooren 2003) and northern Argentina (Chiaramonte 1998). The information about the diet and feeding habits of S. guggenheim along their geographic range remains fragmentary. Vögler et al. (2003) have studied some aspects of S. guggenheim trophic ecology, such as diet diversity and composition, feeding strategy (by sex and size), and diet variability (spatial and seasonal) within the shelf of the Argentine–Uruguayan Common Fishing Zone (AUCFZ). However, changes on S. guggenheim trophic level with growth as well as changes on the trophic level of their prey remain unknown. In addition, the relationship of these changes with type, size and trophic level of prey ingested have not been determined until now. Accordingly, the aims of the present study were: (1) to determine changes in the trophic level of S. guggenheim with increasing body length and (2) to analyze shifts on the type, size and trophic level of prey ingested during the growth of S. guggenheim.

Materials and methods Sample collection Individuals of S. guggenheim were collected from five bottom trawl surveys conducted in spring (December 1995, October 1997) and fall (March 1997, March–

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April 1998, May–June 1998) by the Dirección Nacional de Recursos Acuáticos (DINARA) onboard the RV “Aldebarán”. The surveys used a stratified random sample design and covered most of the AUCFZ (34°00′–39°30′ S; 51°10′–59°10′ W) with a bathymetric range between 3.5 and 266.0 m (Fig. 1). Standard bottom trawls were performed in all surveys with an Engel trawl net (100 mm mesh in the wings and 60 mm mesh in the cod ends, 4 m vertical opening and 15 m horizontal aperture). Each fishing tow lasted 30 min (μ=30, σ=2.40) at a speed of 3.0 knots (μ=2.98, σ=0.14). Only daytime sampling was conducted (from 05:30 to 19:30 h). A total of 1,280 S. guggenheim specimens were captured, counted and weighed (±0.1 kg) on board. During all surveys, 947 S. guggenheim individuals were measured to the lowest cm of total body length (LT), their sex was recorded and the contents of their stomachs were analyzed. The prey were separated and identified to the lowest possible taxonomic level using standard taxonomic keys (Menni et al. 1984; Boschi et al. 1992). Only bony and cartilaginous fish prey of S. guggenheim were measured to the lowest cm of LT. Numerical analysis Cluster analysis was performed to divide the total S. guggenheim sample in length intervals of 5 cm each using the unweighted pairwise group mean average method (UPGMA) with the Euclidean distance as a measure of dissimilarity. Euclidean distance between size groups was calculated as: DðX ;Y Þ ¼

 Xp
2  1=2 X
Y j j i¼1

ð1Þ

where D(X,Y) was the distance between two length groups X and Y; p was the number of length groups; Xj and Yj were the relative importance of prey item j at the length groups X and Y respectively. A Monte Carlo-based ANOSIM procedure (Clarke and Green 1988) was used to test the null hypothesis of no differences in the diet composition between S. guggenheim length groups. This test is based on the rank similarities between samples in the underlying similarity matrix (Clarke and Green 1988). The typifying prey and discriminating prey for each length group were determined using the similarity percent procedure (SIMPER, Clarke 1993). This procedure

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Fig. 1 a The location of the Argentine–Uruguayan Common Fishing Zone (AUCFZ) in South America. b Study area situated inside the AUCFZ. Isobaths of 50, 100, 200 and 400 m are shown. Dots indicate location of fishing tows

determines the average contribution of each prey to the similarity (typifying species) and dissimilarity (discriminating species) between length groups. Bony fish remains and unidentified digested remains were excluded from these analyses. Squatina guggenheim prey were grouped in functional categories according to taxonomic group (mollusc, annelid, crustacean, fish), size (small, medium, large) and habit (pelagic, benthopelagic, demersal) (Table 1). This procedure included each one of the 32 prey identified by Vögler et al. (2003). The contribution of each prey to the diet of S. guggenheim was determined by two Relative Measures of Prey Quantity (RMPQ, after Assis 1996): numerical index (Ni) and frequency of occurrence index (Fi) (Hyslop 1980). A generalized form of the Relative Importance Index (RI) (George and Hadley 1979) was computed for each prey taxon as: RI ¼ 100

Xm

V i¼1 ij

.Xm Xn i¼1

V j¼1 ij



ð2Þ

where Vij is the i-th RMPQ of prey j, n is the number of individuals included in each prey taxon, and m is the number of different prey taxa.

The RI of the functional prey categories was plotted for each length group of S. guggenheim. The level of importance of each prey category was established according with discontinuities in the slope of the RI curve. The categories of prey with high RI values were assigned at the first level of importance and so forth. The trophic level (TL) was calculated for each length group of S. guggenheim applying the methodology proposed by Cortés (1999) as: Xn  TL ¼ 1 þ P  TL ð3Þ j j j¼1 where TL is the trophic level of S. guggenheim (predator), Pj is the proportion of prey taxon j in the predator stomach, TLj is the trophic level of each prey taxon j and n is the number of prey taxon recorded in the predator stomach. In the present study, Pj correspond to numerical index (Ni) values of each prey estimated by Vögler et al. (2003) from S. guggenheim stomach content analysis. TLj values for each prey were obtained from the Sea Around Us Project (Sea Around Us 2006), FishBase (Froese and Pauly 2006) and CephBase (Wood and Day 2006) as of December 2006 (Table 1).

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Table 1 Trophic level, common name and functional category of Squatina guggenheim prey, listed in descending order of trophic level Prey items Mollusca Illex argentinus (Castellanos) Loligo sanpaulensis Brakoniecki Octopus tehuelchus Orbigny Bivalvia (unidentified) Gastropoda (unidentified) Annelida Polychaeta (unidentified) Aphrodita spp. Linnaeus Crustacea Peltarion spinosulum (White) Pleoticus muelleri (Bate) Penaeidae (unidentified) Actinopterygii Percophis brasiliensis Quoy and Gaimard Paralichthys spp. Girard Genypterus brasiliensis Regan Genypterus blacodes (Forster) Cottoperca gobio (Günther) Prionotus nudigula Ginsburg Merluccius hubbsi Marini Cynoscion guatucupa (Cuvier) Helicolenus dactylopterus lahillei (Norman) Urophycis brasiliensis (Kaup) Prionotus punctatus (Bloch) Batrachoididae Dules auriga (Cuvier) Raneya spp. (Kaup) Patagonotothen longipes (Steindachner) Patagonotothen ramsayi (Regan) Trachurus lathami Nichols Conger orbignyanus Valenciennes Paralonchurus brasiliensis (Steindachner) Umbrina canosai Berg Engraulis anchoita Hubbs and Marini Chondrichthyes Squatina guggenheim Marini [23–60 cm LT]

Common name

TL

FC

Argentine shortfin squid Sao Paulo squid Tehuelche octopus Benthic mollusc Benthic mollusc

3.20a 3.20d 3.20d 2.10b 2.10b

MPS SPS SPS SBM SBM

Bristle worms Sea mouse

2.50b 2.50b

SBA SBA

Tractor crab Argentine red shrimp Shrimp

2.52b 2.52b 2.52b

SBC SDC SDC

Brazilian flathead Flounder Cusk-eels Cusk-eels Perch-likes Red searobin Argentine hake Striped weakfish Blackbelly rosefish Brazilian codling Bluewing searobin Toadfishes Cusk-eels Cod icefish Cod icefish Rough scad Argentine conger Banded croaker Argentine croaker Argentine anchovy

4.40a 4.35b 4.34a 4.34a 4.26a 4.20a 4.08a 3.90b 3.81a 3.79a 3.77a 3.67a 3.60a 3.56b 3.49a 3.49a 3.45a 3.40a 3.06a 2.80a 2.48a

MDF MDF LDF LBDF LDF SDF LBPF MBPF MDF MDF MDF MDF SBPF MDF MBPF MBPF MPF LDF SDF MDF SPF

Squatina guggenheim

3.69c

LDF

TL trophic level, FC functional category, SBA small benthic annelids, SBC small benthic crustacean, SBM small benthic mollusc, SBPF small benthopelagic fish, SDC small demersal crustacean, SDC small demersal fish, SPF small pelagic fish, SPS small pelagic squid, MBPF medium benthopelagic fish, MDF medium demersal fish, MPF medium pelagic fish, MPS medium pelagic squid, LBDF large bathydemersal fish, LBPF large benthopelagic fish, LDF large demersal fish a

Froese and Pauly (2006)

b

Sea Around Us (2006)

c

Current study

d

Wood and Day (2006)

According to Vögler et al. (2003) cannibalism in S. guggenheim occurred from larger males to smallest individuals (of both sexes). Then, the TL of S. guggenheim, as a prey, was estimated for the smallest

length group (group I, 23–60 cm) using the methodology proposed by Cortés (1999). The TL for the whole population of S. guggenheim was computed as the average TL estimated for each

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length group and weighted by their relative proportion at the length frequency distribution during the sampling period, as: X TLp ¼ TLi fi ð4Þ where TLp is the trophic level of the population, TLi is the trophic level of the i-th length group and fi is the relative proportion of the i-th length group within the total specimens sampled during the study period. A scatter diagram was plotted to evaluate the relationship between the lengths of prey and predator at the entire body length spectrum of S. guggenheim. The Spearman test (Zar 1999) was performed to establish the significance level (P <0.01) of the regression between the lengths of prey and predator. According with Scharf et al. (2000), prey length data were converted to a ratio scale by dividing each prey length by its corresponding predator length and then plotting these prey length/predator length ratios. The relative frequency distribution and cumulative frequency distribution of prey length/predator length ratios were constructed to evaluate the range of fish prey length eaten by S. guggenheim at their entire body length spectrum. Finally, the total body length (LT) was converted to total body weight (WT) of prey

using length/weight relationships specific to each fish prey as: WT ¼ a  LbT

ð5Þ

where a is the factor and b is the exponent. The values of the parameters a and b where obtained from FishBase home page (Froese and Pauly 2006) for each fish prey. The same procedure was applied to S. guggenheim as predator, however the values of a and b were obtained from Colonello et al. (2007). Then, the weights of fish prey were plotted against predator weight. Only bony fish and cartilaginous fish prey of S. guggenheim were utilised to establish these analyses (Table 2). It was unable to establish the minimum and maximum weights of Paralichthys spp. and Raneya spp., because it was not possible to make a distinction between species within those genera. In turn, data for length and weight of Helicolenus dactylopterus lahillei (Norman), Dules auriga (Cuvier) and Cottoperca gobio (Günther) were not included because the LT of these prey was not measured during sampling on board. The Spearman test (Zar 1999) was performed to establish the significance level (P<0.01) of the regression between the weights of prey and predator.

Table 2 Marine fish prey examined in this study from the stomach contents of Squatina guggenheim Fish prey

LT min (cm)

LT max (cm)

WT min (g)

WT max (g)

Engraulis anchoita Squatina guggenheim Urophycis brasiliensis Conger orbignyanus Paralonchurus brasiliensis Merluccius hubbsi Macrodon ancylodon Cynoscion guatucupa Percophis brasiliensis Trachurus lathami Prionotus punctatus Prionotus nudigula Genypterus spp. Paralichthys spp. Patagonotothen spp. Raneya spp. Cottoperca gobio Dules auriga Helicolenus dactylopterus lahillei

7 29 35 34 10 19 7 5 28 8 12 19 20 8 16 17 – – –

14 29 35 34 20 31 34 25 40 11 12 19 25 15 20 17 – – –

2.81 184.62 354.95 36.71 6.61 68.33 1.88 3.13 90.19 4.68 22.8 78.29 19.62 – – – – – –

31.6 – – – 81.65 231.92 329.98 – 262.68 11.9 – – 43.87 – – – – – –

LT min minimum total body length, LT max maximum total body length, WT min minimum total body weight, WT max maximum total body weight

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Results A total of 947 stomachs of S. guggenheim were examined during the study period at sea and 58.7% (n=552) of them contained food. Three length groups were defined by the cluster analysis, they were based on diet composition: group I (23–60 cm LT), group II (61–80 cm LT) and group III (81–91 cm LT) (Fig. 2). Significant differences (P<0.05) in the diet spectrum were detected by the ANOSIM procedure when compared group I vs II (R=0.87, P=0.005) and group I vs III (R=0.99, P= 0.036). No significant differences (P>0.05) were detected between the diet of group II and III (R= 0.96, P=0.67). Grouping the prey in functional categories showed that small pelagic fishes (i.e. Engraulis anchoita Hubbs and Marini) were the predominant prey item in the diet of smallest individuals of S. guggenheim (group I) and their relative importance decreased in the diet as the body length of predator increase (Fig. 3). In contrast, medium benthopelagic fishes were the most important prey of larger sharks (groups II and III) (Fig. 3). Small demersal crustaceans (shrimps and crabs) had a high relative importance in the diet of sharks included in group II. Medium pelagic squid (i.e. Illex argentinus (Castellanos)) and medium demersal fishes (e.g. Helicolenus dactylopterus lahillei (Norman)) represented secondarily important prey groups in the diet of the largest sharks (group III) (Fig. 3). SIMPER analysis revealed that the diet of the smallest individuals of S. guggenheim (group I) were

Fig. 2 Squatina guggenheim length groups based on diet composition and obtained by a cluster analysis. I, 23–60 cm; II, 61–80 cm; III, 81–91 cm LT

Fig. 3 Relative importance (RI) of functional prey categories (FC) in the diet of Squatina guggenheim length groups (group I, 23–60 cm; group II, 61–80 cm; group III, 81–91 cm LT). Dashed vertical lines indicate the three levels of importance of the functional prey categories according with discontinuities in the slope of the RI curve. The categories of prey with high RI values were assigned at the first level of importance and so forth. Note the different scales in the y-axis between length groups, within the minimum (0) and maximum (100) values of RI. FC abbreviations as showed in Table 1

typified by E. anchoita and Patagonotothen longipes (Steindachner), while in the case of medium sharks (group II) the typified prey were shrimps (Penaeidae), Cynoscion guatucupa (Cuvier) and Merluccius hubbsi Marini. The diet of the largest sharks (group III) was characterised by Patagonotothen ramsayi (Regan) and I. argentinus (Table 3). The diet structure of length groups of S. guggenheim was discriminated by almost the same prey taxa that characterized them. Thus, E. anchoita consistently discriminated the diet between the smallest sharks (group I) and other length groups. In contrast, shrimps (Penaeidae) were the main discriminating prey between the medium sharks (group II) and the other length groups. Finally, I. argentinus and P. ramsayi represented the main discriminating prey between the largest sharks (group III) and the other length groups (Table 4).

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Table 3 Percentage of similarity of typifying (over 5%) prey taxon for the three length groups of Squatina guggenheim Typifying prey taxon

I

II

III

Engraulis anchoita Patagonotothen longipes Penaeidae Cynoscion guatucupa Merluccius hubbsi Patagonotothen ramsayi Illex argentinus

43.26a 16.40a 5.68 5.56

16.50

12.97

14.15

23.29a 22.25a 17.29a

14.65 14.65 21.42a 16.47a

a Prey taxon with higher contribution to the similarity (mean/ SD>4) percentage. I, 23–60 cm; II, 61–80 cm; III, 81–91 cm LT

The size range of fish prey eaten by S. guggenheim expanded with increasing predator body length. Smallest sharks (group I) ingested fish prey ranging from 5 to 21 cm LT (mean=11 cm LT), medium sharks (group II) fed on fish prey between 11 and 35 cm LT (mean=21 cm LT), while largest sharks (group III) consumed fish prey between 13 and 40 cm LT (mean=24 cm LT). The positive relationship between the length of fish prey and the length of S. guggenheim was significant (rs=0.67, P<0.01) (Fig. 4a). The asymmetric relative frequency distribution of prey length/predator length ratios was reflected by two trends where 44.8% and 32.8% of S. guggenheim diet was composed by prey of <20% and >30% of their own body length, respectively (Fig. 4b). Finally, the positive relationship between the weight of fish prey and the weight of S. guggenheim was significant (rs = 0.57, P < 0.01) (Fig. 4c). The trophic level of S. guggenheim increased with increasing body length. Sharks of group I were identified as secondary consumers (TL<4) whereas individuals of groups II and III were tertiary consumers (TL>4) (Table 5). The estimated TL for the whole population of S. guggenheim was 3.90.

Discussion The present study revealed that the relative importance of small pelagic fishes (i.e. E. anchoita) decreased in the diet of S. guggenheim as predator body length increases, while medium benthopelagic fishes (C. guatucupa, P. ramsayi) showed an inverse

tendency. Furthermore, medium pelagic squid (I. argentinus) and medium demersal fishes were important prey categories in the diet of the largest individuals (group III), indicating a broad prey spectrum of S. guggenheim adults. Also, changes in the TL of prey ingested were detected and they were related with functional characteristics (type, size, life habits) of each prey. According to Vögler et al. (2003) bony fishes were the main prey in the diet of the three shark length groups, however, an increase in diet diversity was observed during the growth of S. guggenheim. In many shark species, the increase of body length promotes multiple changes related with movement’s patterns, swimming speed, size of jaws, teeth and stomachs, energy requirements, experience in prey handling, as well as changes in the habitat selection and vulnerability to predation (Wetherbee and Cortés 2004). Increase in body length had promoted changes in the type and size of prey ingested by S. guggenheim and also changes of predator feeding habits were observed. Vögler et al. (2003) observed spatial and temporal variability in S. guggenheim diet diversity. The highest diet diversity was detected in the sharks from shallow depths during spring. In contrast, during autumn the highest diet diversity was observed in sharks from greater depths (Vögler et al. 2003). Therefore, the evidence suggests that prey availability differs in space (between depths) and time (between seasons) within the shelf of the AUCFZ. In this context, E. anchoita was the main prey of S. guggenheim, as well as I. argentinus and M. hubbsi

Table 4 Percentage of dissimilarity of discriminating (over 5%) prey taxon for the three length groups of Squatina guggenheim Discriminating prey taxon

I vs II

I vs III

Engraulis anchoita Patagonotothen longipes Penaeidae Cynoscion guatucupa Merluccius hubbsi Bivalvia Patagonotothen ramsayi Illex argentinus Helicolenus dactylopterus lahillei

11.81a 7.14a 6.96a 7.25a 6.42a 6.49 7.99

6.31a 8.79a

a

II vs III

7.25a 5.45 5.42 6.46a 8.70a 7.79a

5.48 12.37a 6.86a 6.78a

Prey taxon with higher contribution to the dissimilarity (mean/ SD>2) percentage. I, 23–60 cm; II, 61–80 cm; III, 81–91 cm LT

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November with some spawning activity in the southern coastal zone of the continental shelf at depths <100 m in the Buenos Aires (Argentina) sector of the AUCFZ (Bakun and Parrish 1991). Merluccius hubbsi spawns between autumn and winter in the north of the AUCFZ (Norbis et al., 1999), and I. argentinus spawns in this same area during winter and spring (Bazzino and Quiñones 1999). The AUCFZ is influenced by four water masses (Acha et al. 2004), namely: the Brazil Current (warm water); the Malvinas Current (cold water); the Patagonia Current (cold water), and Río de la Plata discharges (freshwater) (Guerrero et al. 1997). The Brazil (Subtropical) and Malvinas (SubAntarctic) Currents meet, on average, at 36° S, generating the ‘Subtropical Convergence’, a large permanent frontal system of high temporal variability that is displaced northward in winter and southward in summer (Olson et al. 1988). The flow of the Río de la Plata changes seasonally discharging freshwater along the Uruguayan coast during winter and along the Argentinean coast in spring and summer (Guerrero et al. 1997). The dynamic interaction of these water masses promotes seasonal and spatial variability of temperature and salinity in the AUCFZ, which could influence the distribution of S. guggenheim and their prey, promoting an overlap between them both in space and in time. Vögler et al. (2003) operationally grouped S. guggenheim specimens in three length groups. Here, also three length-related groups were elucidated using a formal statistical procedure. The length groups defined in the two studies were different, but both have detected changes of prey relative importance with the increase of S. guggenheim body length. Fig. 4 a Lineal regression between total body length of prey (prey LT, cm) and total body length of predator (predator LT, cm) at the entire length spectrum of Squatina guggenheim. b Relative frequency distribution (bars) and cumulative frequency distribution (continuous line, filled dots at 5% intervals) of prey length/predator length ratios. c Lineal regression between total body weight of prey (prey WT, g) and total body weight of predator (predator WT, g) at the entire weight spectrum of S. guggenheim. At a and c dashed lines indicate ±95% confidence interval of Spearman test (rs)

were secondary preys (Vögler et al. 2003). The seasonal distribution of these species within the AUCFZ was related to their reproductive biology. For example, E. anchoita spawns from September to

Table 5 Trophic level of the three length groups of Squatina guggenheim Length group

TL

N

n

I II III

3.69 4.26 4.40

342 145 65

415 199 93

I, 23–60 cm; II, 61–80 cm; III, 81–91 cm LT TL Trophic level N number of stomachs with food contents, n total number of prey found in the stomachs of each length group

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The feeding strategy that characterizes many carnivorous fishes reflects that prey size increase with the increase of predator body length (Karpouzi and Stergiou 2003). This kind of relationship is consistent with an asymptotic relationship between TL and LT of fish (Cortés 1999; Stergiou and Karpouzi 2002). However, in the case of S. guggenheim the asymmetric relative frequency distribution of prey length/ predator length ratios suggest that this predator incorporates a considerable number of intermediate length prey in their diet while it also continues to feed on several small prey during the growth. Scharf et al. (2000) have demonstrated that this kind of prey length/predator length relationship is a common characteristic of many fish predators’ diet and contrasts with optimal foraging theory (Stephens and Krebs 1986), which predicts that the largest prey available should be eaten to maximize feeding efficiency. It is important to note that the present analysis only included teleost and cartilaginous fish prey. Throughout the growth, the diet of S. guggenheim was in general more concentrated on fish, rather than on invertebrates (Vögler et al. 2003) but significant differences (P≤0.05) between the diet of three length groups were found. Further studies are necessary to elucidate the cause of the differences in the diet between length groups with the incorporation of length and weight of other prey groups (i.e. crustaceans, molluscs and annelids). Food and feeding habits determine the position of animals within food webs, and define their ecological role (Pauly et al. 1998). Changes in food and feeding habits of sharks during growth are reflected in their accessibility to prey available or in the improved capacity of larger sharks to capture different prey (Graeber 1974; Weihs et al. 1981; Stillwell and Kohler 1982; Lowe et al. 1996). Shifts in the TL of shark species with growth have not been quantified until the present. The current study represents the first evidence in this sense, revealing important changes of S. guggenheim TL throughout their growth. When the population was split into length groups (based on diet composition), the smallest sharks (23–60 cm LT) were identified as secondary consumers (TL <4) whereas medium sharks (61– 80 cm LT) and largest sharks (81–91 cm LT) were placed as tertiary consumers (TL>4). The increase in diet diversity and the shifts in type, size, and TL of

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prey ingested by S. guggenheim place this predator at higher trophic levels as it grows. However, S. guggenheim (TL=3.90, current study) cannot be considered a top predator because it is, in turn, preyed upon by other larger sharks such as Carcharhinus brachyurus (Günther) (TL=4.2, Cortés 1999), Carcharias taurus Rafinesque (TL=4.4, Cortés 1999) (Lucifora 2003) and Notorynchus cepedianus (Péron) (TL=4.7, Cortés 1999) (Lucifora et al. 2005). According with Cortés (1999) the trophic levels of sharks ranged from 3.1 in Stegostoma fasciatum (Hermann) to 4.7 in N. cepedianus. Thus, as a species S. guggenheim is a secondary consumer (TL<4) and their predators are tertiary consumers (TL>4) in the food webs in which these sharks occur. S. guggenheim TL estimated by the current study agrees well with the values reported by Cortés (1999) for six other species of Squatina. However, it’s important to note that the current study was population-based, which allowed a more precise estimate of TL since it was supported by the observed population length frequency distribution (sample size= 1280 sharks; unpublished data). The TL of the whole population should be considered as a population “health” indicator since it summarizes changes in population dynamics, prey availability and predator–prey interactions. Then, if the whole population TL of S. guggenheim was less than 3.90 (as reference point) this will be indicative of a decrease of the adult fraction, or an increase in the juvenile fraction of the population or/and a change in the environmental prey availability. Thus, the periodic estimation of the whole population TL would be a useful indicator to identify changes in the population size structure brought about by fishing, natural phenomena or other causes, which could impact the predation pressure exerted by S. guggenheim, and with it the consequent modification of the trophic flow between components of the coastal marine community. The trophic implications of removing this predator from the coastal marine ecosystem of the AUCFZ remain unknown. Trophic models have been long recognized as useful computational tools to elucidate the trophic position of the species into the food web and even to identify the species trophic roles within a marine ecosystem (e.g. Christensen and Pauly 1992; Walters et al. 1997; Cury et al. 2000; Pauly et al. 2000; Christensen and Walters 2004). However, trophic models do not usually split top predators, such as

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sharks or marine mammals, according with developmental stages or length groups (e.g. Stevens et al. 2000). The evidence presented here indicates that, in order to obtain a more realistic representation of the structure and dynamics of marine food webs, trophic models necessarily should consider changes in the trophic level that occur during the growth of sharks. It is evident that a single method of stomach analysis cannot give a complete picture of diet composition. In order to glean the maximum amount of information from the material, the prudent investigator should employ at least one method measuring the amount, and one measuring the bulk of food material present (Hyslop 1980). This study did not use volumetric or gravimetric methods to measure the bulk of the food material. Nevertheless, it is considered that the two methods employed here to record the amount of food material (i.e. occurrence and numerical methods) are good approximations in order to study the diet composition of S. guggenheim, taking into account that: (a) is a carnivorous predator that swallows its prey whole and, (b) on board identification of prey items from stomach contents was feasible.

Summary Changes in the trophic ecology of S. guggenheim were detected with its growth. First, shifts in the type, size, life habits and TL of prey ingested were identified. Second, the size range of prey expanded with increasing predator body length. Third, the increase of mean prey weight was positively correlated with the increase of S. guggenheim weight. Lastly, switches of S. guggenheim TL through its growth were quantified. Interactions between prey (type, size, TL) and predator (length, weight) characteristics explain the increase in S. guggenheim TL as this predator grows larger.

Acknowledgments The authors thank DINARA (Uruguay) for permitting us to generate the database used in this research through the participation of R.V.S and A.C.M. in regular Micropogonias furnieri and Merluccius hubbsi evaluation cruises. We also acknowledge the crew of the RV “Aldebarán” for their assistance. B. Yannicelli, E. Cortés and L. Lucifora provided useful comments to improve the manuscript. The German Academic Exchange Service (Deutscher Akademisher

Environ Biol Fish (2009) 84:41–52 Austausch Dienst, DAAD) funded R.V.S. (A/99/14455) and A. C.M. (A/01/17601) through scholarships to conduct graduate studies at the University of Concepción.

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