No bull: Juvenile bull sharks may play diverse functional roles in coastal food webs. Aaron J. Wirsing
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1 No bull: Juvenile bull sharks may play diverse functional roles in coastal food webs Aaron J. Wirsing
2 Introduction Predators may induce numerous direct and indirect effects in food webs Most studies of these effects have used a species based approach i.e., individuals within a predator species have same trophic niche* (network of trophic interactions) This approach could mask important variation in the way predator individuals affect community and ecosystem properties *Elton (1927) Animal Ecology
3 Introduction e.g., just five killer whale individuals (Orcinus orca) switching their diets from pinnipeds to sea otters (Enhydra lutris) may have triggered declines in otter populations* that ultimately led to collapse of kelp ecosystems in the northeastern Pacific *Williams et al. (2004) Ecology Es tes et al. (1998) Science
4 Introduction Studies addressing possibility that top down effects might vary as function of individual differences in trophic interactions needed First step: document among individual trophic niche variation Juvenile bull sharks in an undeveloped subtropical estuary
5 The Bull Shark Brian Skerry (Nat geo) Shallow tropical/subtropical distribution Large: to 3.4 m (~11 ft) Broad diet (teleosts, marine mammals, sharks) Threat to humans Euryhaline
6 Bull Sharks in Fresh Water Brian Skerry (Nat geo) Females venture into estuaries to pup Neonates and juveniles continue to use freshwater Explanation Safety from larger sharks Our questions Do juvenile sharks feed on freshwater resources while upstream? If so, is there variation with respect to this tendency?
7 Shark River Estuary N Upstream Downstream Mid estuary Gulf of Mexico Mouth 5 km Florida Coastal Everglades
8 Longline Sampling ca. 500m longline equipped with 50 Mustad size 12/0 tuna circle hooks
9 Fishing Protocol Sampling allocated evenly across 4 sites, seasons Longlines deployed from dawn to dusk Soak time = 1 hour Bull sharks caught processed immediately
10 Handling Protocol All sharks Tagged, measured, sexed Muscle tissue sample collected using biopsy punch (0.5 cm 2, lateral to first dorsal fin)
11 Stable Isotopic Analysis Muscle samples used to generate stable carbon (C) and nitrogen (N) isotopic signatures Stable isotopic analysis: provides time and space integrated representation of trophic ecology Ratios of nitrogen isotopes ( 15 N to 14 N, or δ 15 N) exhibit stepwise enrichment with trophic transfers, estimate trophic position Ratios of carbon isotopes ( 13 C to 12 C, or δ 13 C) vary among primary producers but not trophic transfers, identify ultimate sources of dietary carbon (trophic niche) Bull shark muscle tissue turnover rate: 100s of days δ 15 N & δ 13 C identify long term differences in resource use ANOVA to test for effects of length, sex, season, site on δ 15 N, δ 13 C
12 Defining Food Web Endpoints Goal: Determine extent to which juvenile bull sharks feed in freshwater vs. marine food webs Defined ranges of δ 13 C representative of producers and consumers existing solely in freshwater and marine food webs Establishment of isotopic carbon boundaries ( endpoints ) to distinguish sharks feeding exclusively in marine or freshwater food webs from those in both
13 Defining Food Web Endpoints Endpoint Freshwater food web Both food webs Endpoint Marine food web δ 13 C (Entire Range)
14 Results Muscle tissue samples from 79 juvenile bull sharks Largest reported database of stable isotope values for any elasmobranch Sizes ranged from 72 to 190 cm (total length) 1:1 sex ratio
15 Mean Isotopic Ratios for Bull Sharks No significant variation in stable nitrogen isotope (δ 15 N) signatures with respect to length (F 1,78 =0.24, P = 0.6) sex (F 1,78 =0.76, P = 0.8) season (wet versus dry) (F 1,78 =0.61, P = 0.4) site (F 3,78 =0.44, P = 0.7)
16 Mean Isotopic Ratios for Bull Sharks Juvenile bull sharks Trophic Position Source of Dietary Carbon ( Freshwater vs. Marine)
17 Mean Isotopic Ratios for Bull Sharks No significant variation in stable carbon isotope (δ 13 C) signatures with length (F 1,78 =1.76, P = 0.2) sex (F 1,78 =2.90, P = 0.1) season (F 1,78 =1.41, P = 0.2) But, sharks captured at the mouth of estuary were more 13 C enriched than those caught at sites farther upstream (F 3,78 =7.60, P = )
18 Mean Isotopic Ratios for Bull Sharks Juvenile bull sharks Trophic Position In Estuary: Mixed diet At Mouth: Marine diet Source of Dietary Carbon ( Freshwater vs. Marine)
19 Individual Isotopic Ratios
20 Trophic Niche Differentiation i.e., exploration of individual signatures revealed Three Niches (1) Specialized niche: reliance on marine resources (2) Generalized niche: mixed diet (3) Specialized niche: reliance on freshwater resources Would have been missed had we relied on mean signatures
21 Distribution of Trophic Niches Downstream Mouth Upstream Gulf of Mexico Mid-estuary Trophic Niche: Marine (Blue) Mixed (Green) Freshwater
22 Summary Juvenile bull sharks manifest 3 tropic niches Two specialized, one generalized Specialized freshwater niche missed without focus on individuals Niche variation not explained by size, sex, seasonal fluctuation Trophic niches showed little spatial segregation
23 Implications (1) Juvenile bull sharks as vectors of nutrients into the nutrient limited upper reaches of the Shark River e.g., P Loss of bull sharks could alter upstream nutrient dynamics (2) Reliance on a small sample of individuals and/or a focus on mean trends could mask the diverse functional roles that predators play (3) Ecological consequences of declines in large predators may be greater than is appreciated Loss of bull sharks could alter top down forcing in marine and freshwater food webs
24 Acknowledgements Collaborators Michael Heithaus Bryan Delius Special thanks also to Derek Burkholder Katy Cameron Jim Fourqurean Adam Rosenblat Jeremy Vaudo Craig Layman Meagan Dunphy Daly
25 A Trade off? Intraspecific variation in trophic niches can stem from unique set of trade offs being associated with each niche* Likely the case for bull sharks in the Shark River Marine river mouth is resource rich but dangerous (predation by larger bull and lemon sharks) Inside estuary, resources more scarce but predation risk is low This food safety trade off would promote niche diversity by Allowing some individuals to exploit limited freshwater resources upstream in safety While driving others to risk predation downstream for greater reward *Bolnick et al. (2007) PNAS Lemon shark (Negaprion brevirostris)
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