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Quantifying shark predation effects on prey: Dietary data limitations and study approaches

March 2019
Endangered Species Research 38:147-151

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Understanding the ecological impacts of sharks on prey populations has become a research priority given widespread shark population declines due to overfishing, combined with significant conservation efforts. Accordingly, many studies have conducted analyses of shark stomach contents and/or used biomarkers, such as stable isotope signatures, to assess dietary pat-terns in order to infer ecological roles. Here, I summarize how relying on stomach contents and/or stable isotope signatures to assess the potential for sharks to initiate trophic cascades can be misleading and may significantly underestimate the strength of shark top-down predation effects on prey. However, a study approach that measures attributes of the sharks (e.g. hunting mode), potential prey (e.g. escape speed) and the environment (e.g. habitat rugosity) can provide greater insights for quantifying the magnitude of top-down predation effects of sharks and the potential for their population declines or recoveries to trigger trophic cascades. To aid future investigations,I provide a set of predictions, based on ecological theory, which would specifically lead to increases in the magnitude of shark predation effects on prey populations. I also present key study approaches currently being employed by researchers to test such predictions.

Conceptual diagram of how expression of antipredatory responses by prey can increase risk effects of predators, while reducing direct predation mortality (adapted from Creel & Christianson [2008]). Consider 3 prey species (α, β, and φ) that become exposed to increasing densities of predators. In such a scenario, (A) individuals of surviving prey α, β, and φ may exhibit antipredatory responses (e.g. induce defensive armor or hiding behavior) that scale with their respective level of encounter rates with attacking predators. However, (B) if φ increases its expression of antipredator traits effectively, direct predation will decrease on φ and consequently φ will become rare or absent in predator diets, although predators still have strong risk effects on φ. Moreover, if antipredatory responses of φ cause predators to shift their hunting efforts towards α and β, then (C) direct effects and risk effects can even become negatively correlated

…

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ENDANGERED SPECIES RESEARCH

Endang Species Res

Vol. 38: 147–151, 2019

https://doi.org/10.3354/esr00950 Published March 28

1. INTRODUCTION

Both ecological theory and empirical data demon-

strate that predators can affect prey communities, and

subsequently initiate trophic cascades, even in the

absence of prey consumption (Creel & Christianson

2008, Estes et al. 2016, Hammerschlag et al. 2019).

However, some recent discussions on the ecological

roles of sharks have been increasingly focused on

aspects of diet (e.g. Grubbs et al. 2016, Roff et al. 2016,

Bond et al. 2018). For example, when evaluating for

the potential for shark declines to initiate trophic cas-

cades, Grubbs et al. (2016) argued that 5 criteria need

to be considered, among them being that prey be a sig-

nificant part of a predator’s diet and also that the pred-

ator be the primary source of prey predation mortality.

In light of these discussions, the goal of this paper is to

evoke relevant ecological theory to demonstrate that

relying on dietary information can be misleading when

trying to quantify the strength of top-down predation

effects of sharks, and consequently, the potential for

their population declines or recoveries to initiate

trophic cascades. To aid in future investigations into

shark ecological roles, I also provide a set of predic-

tions, based on functional attributes of sharks, prey

and the environment, which would lead to increases in

the magnitude of shark predation effects on prey pop-

ulations. I also review key study approaches currently

being employed to quantify effects of sharks on prey. I

note upfront that because the ecological concepts

being cited here have already been reviewed else-

where, I will not do so again in this paper.

Attribution Licence. Use, distribution and reproduction are un -

restricted. Authors and original publication must be credited.

Publisher: Inter-Research · www.int-res.com

*Corresponding author: nhammerschlag@miami.edu

OPINION PIECE

Quantifying shark predation effects on prey:

dietary data limitations and study approaches

Neil Hammerschlag1,2,*

1Rosenstiel School of Marine and Atmospheric Science, University of Miami, Miami, FL, 33149, USA

2Leonard and Jayne Abess Center for Ecosystem Science and Policy, University of Miami, Coral Gables, FL, 33146, USA

ABSTRACT: Understanding the ecological impacts of sharks on prey populations has become a

research priority given widespread shark population declines due to overfishing, combined with

significant conservation efforts. Accordingly, many studies have conducted analyses of shark

stomach contents and/or used biomarkers, such as stable isotope signatures, to assess dietary pat-

terns in order to infer ecological roles. Here, I summarize how relying on stomach contents and/or

stable isotope signatures to assess the potential for sharks to initiate trophic cascades can be mis-

leading and may significantly underestimate the strength of shark top-down predation effects on

prey. However, a study approach that measures attributes of the sharks (e.g. hunting mode),

potential prey (e.g. escape speed) and the environment (e.g. habitat rugosity) can provide greater

insights for quantifying the magnitude of top-down predation effects of sharks and the potential

for their population declines or recoveries to trigger trophic cascades. To aid future investigations,

I provide a set of predictions, based on ecological theory, which would specifically lead to in -

creases in the magnitude of shark predation effects on prey populations. I also present key study

approaches currently being employed by researchers to test such predictions.

KEY WORDS: Shark · Apex predator · Predation risk · Trophic cascade · Coral reef · Fishing

PEN

CCESS

Endang Species Res 38: 147–151, 2019

148

2. LIMITATIONS OF DIETARY INFORMATION

Besides the well known limitations of gut content

analyses (reviewed by Baker et al. 2014), there are

various reasons why assessments of trophic levels or

ecological roles of sharks, in particular, cannot rely

primarily on this method. First, shark stomachs are

usually empty as they often evert their stomach upon

capture for sampling (Brunnschweiler et al. 2011). Sec-

ond, while sharks and other predators can most obvi-

ously affect prey by killing and consuming them, pred-

ators can also initiate strong top-down effects on prey

even when prey are absent from predator stomachs

and the direct predation mortality to prey is zero (re-

viewed in Creel & Christianson 2008). This is because

antipredator responses of prey, and associated risk ef-

fects, will lower direct predation mortality and as a re-

sult, prey will be rare or even absent in the stomach of

predators (Creel & Christianson 2008; Fig. 1).

In addition to stomach content analysis, stable iso-

tope signatures of nitrogen (N) and carbon (C) from

tissues are increasingly being used to infer trophic

niches of sharks (reviewed by Hussey et al. 2012,

Shiffman et al. 2012). There are many considerations

and limitations when applying this tool to study the

trophic ecology of individuals or populations (see re-

views by Layman et al. 2012); yet, many studies con-

tinue to use isotopic ratios from tissues to estimate

trophic position of sharks relative to other species in

the community and subsequently infer ecological

roles. However, among other possible issues, stable

isotope signatures are a long-term integration of re-

sources and it is possible that 2 species can have dis-

tinct diets but very similar isotopic signatures, if one

consumer’s isotopic signature represents the average

of 2 isotopically extreme resource bases. This is par-

ticularly relevant in the case of sharks since they are

opportunistic trophic omnivores, feeding across the

food web and among different habitats (Hussey et al.

2012, Shiffman et al. 2012). Accordingly, studies that

rely primarily on diet and stable isotope information

may underestimate top-down effects of sharks.

In a recent review, Roff et al. (2016) argued that

large reef sharks are trophically equivalent to sym-

patric piscivorous teleosts, such as large groupers and

snappers. They further concluded that the removal of

reef sharks by humans is therefore unlikely to initiate

strong top-down effects on large teleosts and therefore

unlikely to trigger trophic cascades. These arguments

were largely based on 2 primary lines of reasoning.

First, large piscivorous teleosts are often rare or

absent in the diet of sampled reef sharks. Second, sta-

ble isotope signatures generally overlapped between

reef sharks and these large piscivorous tele osts. How-

ever, these arguments did not take into account the

limitations of relying solely on studies of diet and sta-

ble isotopes to infer strengths of top-down predator

effects as described above. These limitations are evi-

denced by recent data which suggest that the

targeted removal of large-bodied reef sharks has con-

tributed to changes in the abundance, di-

versity, diet, condition and morphology

of coral reef fishes (Ruppert et al. 2013,

2016, Barley et al. 2017a,b, Hammer-

schlag et al. 2018).

3. APPROACHES FOR QUANTIFYING

SHARK PREDATION EFFECTS

Several papers have developed frame-

works for determining the strength of

predator effects on prey populations.

Taken together, these works have

shown that functional attributes of the

predator (e.g. hunting mode), prey (e.g.

grouping) and the environment (e.g.

habitat structure) can influence the

outcome of predator−prey interactions

(Schmitz 2008, Creel 2011, 2018,

Schmitz et al. 2017, Gaynor et al. 2019).

By synthesizing these works in combi-

nation with an understanding of preda-

Fig. 1. Conceptual diagram of how expression of antipredatory responses

by prey can increase risk effects of predators, while reducing direct preda-

tion mortality (adapted from Creel & Christianson [2008]). Consider 3 prey

species (α, β, and φ) that become exposed to increasing densities of preda-

tors. In such a scenario, (A) individuals of surviving prey α, β, and φmay

exhibit antipredatory responses (e.g. induce defensive armor or hiding

behavior) that scale with their respective level of encounter rates with

attacking predators. However, (B) if φincreases its expression of antipreda-

tor traits effectively, direct predation will decrease on φand consequently φ

will become rare or absent in predator diets, although predators still have

strong risk effects on φ. Moreover, if antipredatory responses of φcause

predators to shift their hunting efforts towards α and β, then (C) direct

effects and risk effects can even become negatively correlated

Hammerschlag: Quantifying shark predation effects

tor−prey interactions involving sharks based on my

own in situ studies, I provide a set of predictions that

would specifically lead to increases in the magnitude

of shark predation effects on prey, and distinguish

whether consumptive or risk effects would dominate

these interactions. These are listed in Table 1 and

may be useful for identifying potential situations

where sharks can affect prey through either con-

sumptive or risk effects.

There are a variety of methodological approaches

already being used for measuring relative attributes

of sharks, prey and the environment at appropriate

scales for assessment of shark predation effects. Rel-

evant shark attributes for investigation include

assessing their hunting mode (search and pursuit vs.

sit and wait), hunting periods, hunting areas, group-

ing, feeding rates, and gape size. For example, using

underwater visual surveys, Robbins & Renaud (2016)

documented differences in hunting strategies and

predation success rate among grey reef sharks,

Carharhinus amblyrhynchos, at Fakarava Atoll,

French Polynesia. During morning hours, the sharks

targeted spawning grouper, employing burst speed

to capture fish engaged in spawning. In contrast,

sharks switched prey targets to other fish species at

night, employing a slow, controlled approach which

minimized the distances between sharks and prey

fish prior to any predation attempts (Robbins &

Renaud 2016). These differences in hunting strategy

appeared to be related to the mobility of the different

species being targeted and the different environ-

mental conditions (day vs. night). When direct obser-

vation of shark hunting is not possible, as is usually

the case, multi-sensor biotelemetry and biologging

tools are particularly valuable for remotely recording

this aspect of shark behavior (Hussey et al. 2015).

This could include combining shark tracking with

accelerometers (Papastamatiou et al. 2018b), preda-

tion tags (Halfyard et al. 2017) and animal-borne

cameras (Papastamatiou et al. 2018a).

There are numerous relevant behavioral, physio-

logical and morphological attributes for investigating

149

Focus Attribute and prediction

Shark Both RE and CE will be high when sharks hunt in packs or hunt individually, but simultaneously

Both RE and CE will be high when sharks have a sensory advantage over prey (e.g. increased visual

acuity under low light conditions)

Both RE and CE will be high when sharks have a cognitive advantage over prey (e.g. when they exhibit

social learning or can refine hunting strategy over time)

RE will be higher than CE for ambush predatory sharks which require specific forms of habitat for cover

CE will be higher than RE for active or coursing predatory sharks that do not associate with specific forms

of habitat for cover

RE will be higher than CE when sharks are abundant and predictably distributed

CE will be higher than RE when sharks are widespread or rare

Prey RE and CE will be high for prey that do not employ grouping or schooling behavior or during periods

where they exhibit reduced group or school size

RE will be higher than CE in dietary generalists that can shift habitats in response to sharks

CE will be higher than RE in dietary specialists that cannot alter feeding habits in response to sharks

RE will be higher than CE for prey that can alter or adapt morphological traits in response to sharks

CE will be higher than RE for prey that cannot alter or adapt morphological traits in response to sharks

CE will be higher than RE when prey spatially or temporally aggregate to exploit a predictable temporal

resource pulse, such as an ephemeral food source

CE will be higher than RE when prey spatially or temporally aggregate to engage in a critical life history

event that increases population fitness (e.g. spawning or mating)

RE will be higher than CE when prey have advanced cognition and sensory perception

Environment RE will be higher than CE in more heterogenous environments where prey have more options to hide or

take refuge, such as reefs with high rugosity or dense kelp beds that exclude sharks

CE will be higher than RE in more homogeneous environments were prey have limited options to hide or

take refuge, such as open sand flats

RE will be higher than CE under environmental conditions that offer prey increased ability to detect

predators, such as good water visibility and during daylight hours

CE will be higher than RE under environmental conditions in which prey have reduced ability to detect

predators (e.g. low light, high turbidity)

Table 1. Predicted attributes of sharks, prey and the environment leading to increases in the magnitude of shark top-down

predation effects on prey, and whether consumptive effects (CE) or risk effects (RE) dominate these interactions. Predictions

developed from synthesizing works of Schmitz (2008), Creel (2011, 2018), Schmitz et al. (2017), and Gaynor et al. (2019), in

combination with an understanding of predator−prey interactions involving sharks based on my own experiences

Endang Species Res 38: 147–151, 2019
150
antipredatory responses in prey. These include
schooling or grouping behavior, escape mode, space
or time devoted to vigilance or refuge use, excursion
distances and activity space (in 3 dimensions), forag-
ing rates, body mass and condition, movement rate,
stress levels, nutritional condition, and morpho -
logical structures associated with defense, detection,
or evasion. As in the case for sharks, behavioral re-
sponses of prey could be measured via observational
and/or biotelemetry and biologging tools (Wirsing et
al. 2007, Madin et al. 2010, De Vos et al. 2015). For
example, using underwater camera monitoring on
Australian coral reefs, Atwood et al. (2018) measured
grazing rates of herbivorous fishes at varying dis-
tances from refuges under threat of predation. Physi-
ological responses of prey could be assessed non-
 invasively via tissue or scat sampling (Hammerschlag
et al. 2017, Oliveira et al. 2017). Morphological re-
sponses include measuring shape and size of preda-
tory defense structure (e.g. claws or spines; Miller et
al. 2015), detection structures (e.g. eyes, olfactory
bulbs; Smith & Litvaitis 1999, Møller & Erritzøe 2014),
and/or evasive locomotory structures (e.g. flipper or
fins; Hammerschlag et al. 2018).  Relevant environ-
mental attributes widely found to decrease predation
risk include increased habitat complexity (Schmitz
1998), proximity to refuge (Atwood et al. 2018), and
visibility (Hammerschlag et al. 2006) as well as de-
creased depth (Rypel et al. 2007). These environmen-
tal attributes can be measured in situ or via remotely
sensed data (e.g. Madin et al. 2011).
In terms of an experimental approach, these pred-
ator−prey attributes can be investigated under natu-
ral conditions in response to temporal and/or spatial
variation of hunting sharks (e.g. Wirsing et al. 2007,
Hammerschlag et al. 2012) or with introduced model
sharks (Madin et al. 2010, Rizzari et al. 2014). An
emerging opportunity are comparisons over time or
between areas exposed to differences in targeted
shark removals or protections (e.g. Barley et al.
2017a,b, Speed et al. 2018). In addition to these field-
based approaches, mesocosom or laboratory experi-
mentation of prey reactions to predators are valuable
for understanding the often cryptic nature of interac-
tions between shark and their prey (Bedore et al.
2015, Barrios-O’Neill et al. 2017, Stump et al. 2017).
4.  CONCLUSION
In summary, relying on stomach contents and/or stable
isotope signatures to assess the potential for sharks to
initiate trophic cascades can be misleading and may
significantly underestimate the strength of shark top-
down predation effects on prey. A study approach that
measures relevant functional attributes of sharks, prey
and the environment can provide greater insights for
quantifying the magnitude of top-down predation
effects (Schmitz 2008, Creel 2011, 2018, Schmitz et al.
2017, Gaynor et al. 2019) and the potential for shark
population declines or recoveries to trigger trophic cas-
cades. As outlined by Ruppert et al. (2016), there is a
need for research efforts to focus on predator−prey
relations (rather than simply the ecology of the preda-
tor) to understand the process of predation.
Acknowledgements. Thanks to Brendan Godley, who en -
couraged me to submit this work, and to the anonymous
reviewers whose comments helped significantly strengthen
this paper. I also thank the many great colleagues whose
research laid the groundwork for this paper and enabled me
to synthesize the ideas presented.
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Nov 2022

The stomach contents of 30 male and 43 female (age < 3 years; 74–236 cm total length) juvenile great hammerhead sharks (Sphyrna mokarran (Rüppell, 1837)) obtained from commercial fisheries operating in Saudi Arabian waters of the Arabian Gulf were analyzed for the first time. After exclusion of parasites and abiotics, a total of 31 prey items, including the remains of cephalopods, fish, crustaceans, and bivalve mollusks, were identified in the stomachs of 59 great hammerheads. Based on the index of relative importance, teleosts were their main prey, and Platycephalus indicus (Linnaeus, 1758) was the most important prey at the species level. Significant age-related dietary differences were noted (F = 1.57, p = 0.026), indicating that the prey of the hammerheads aged 0–3 years shifted from Platycephalidae to Myliobatidae. Levin’s niche overlap index was low (0.05–0.21), indicating that <3-year-old juvenile great hammerheads are specialized predators. The estimated trophic level was 4.40–5.01 (mean ± SD, 4.66 ± 0.45), indicating that the great hammerhead is a tertiary consumer.

Trophic-Mediated Pelagic Habitat Structuring and Partitioning by Sympatric Elasmobranchs

Article

Full-text available

Jun 2022

Pelagic elasmobranchs are key elements of oceanic ecosystems and must be preserved if marine trophic networks are to be kept in balance. Yet, they face intense fishing pressure that has been threatening their populations worldwide. Ensuring proper conservation management of these taxa depends on a better understanding of the strategies they use to explore the pelagic realm and their contributions to trophic web structuring across the ocean column. This study aimed at examining relationships between vertical habitat use and trophic attributes among six sympatric pelagic elasmobranchs using satellite transmitting tags in the western equatorial South Atlantic Ocean. The vertical movements of 35 elasmobranch individuals were tracked during an overall total of 1911 days. Clear relationships between species’ feeding habits, maximum diving depths, and proportion of time spent either in epipelagic or in surface waters were evidenced by Bayesian generalized linear mixed models and multivariate analysis. Filter-feeders made most use of deep waters from the mesopelagic and bathypelagic and shifted their diving depths in phase with diel vertical migrations of the deep scattering layer, i.e., shallower during the night and deeper during the day. Specialists exhibited distinct diving patterns in epipelagic and mesopelagic waters across the diel period which are potentially indicative of habitat partitioning, whereas generalists were more surface-oriented but also explored deeper waters compared to specialists. The trophic level also seemed to influence elasmobranch maximum diving depths, which tended to become shallower as species’ trophic level increased. These results corroborate previous evidence of widespread vertical habitat partitioning among sympatric pelagic predators and depict a trophic-mediated structuring of the pelagic environment where top-down control may be exerted at different depths by distinct species. Further research is yet required to understand the role of elasmobranch vertical movements in structuring pelagic habitats as well as to guide ecosystem-based fisheries management aimed at reducing species susceptibility to fishing gear and at preserving the structure and functionality of marine trophic networks.

Emerging insights on effects of sharks and other top predators on coral reefs

Article

Full-text available

Mar 2022

Predation is ubiquitous on coral reefs. Among the most charismatic group of reef predators are the top predatory fishes, including sharks and large-bodied bony fishes. Despite the threat presented by top predators, data describing their realized effects on reef community structure and functioning are challenging to produce. Many innovative studies have capitalized on natural experimental conditions to explore predator effects on reefs. Gradients in predator density have been created by spatial patterning of fisheries management. Evidence of prey release has been observed across some reefs, namely that potential prey increase in density when predator density is reduced. While such studies search for evidence of prey release among broad groups or guilds of potential prey, a subset of studies have sought evidence of release at finer population levels. We find that some groups of fishes are particularly vulnerable to the effects of predators and more able to capitalize demographically when predator density is reduced. For example, territorial damselfish appear to realize reliable population expansion with the reduction in predator density, likely because their aggressive, defensive behavior makes them distinctly vulnerable to predation. Relatedly, individual fishes that suffer from debilitating conditions, such as heavy parasite loads, appear to realize relatively stronger levels of prey release with reduced predator density. Studying the effects of predators on coral reefs remains a timely pursuit, and we argue that efforts to focus on the specifics of vulnerability to predation among potential prey and other context-specific dimensions of mortality hold promise to expand our knowledge.

Predation of archival tagged Dolly Varden, Salvelinus malma, reveals predator avoidance behaviour and tracks feeding events by presumed beluga whale, Delphinapterus leucas, in the Beaufort Sea

Article

Full-text available

Dec 2021

Background We report compelling evidence suggesting a predation event of a pop-up satellite archival tagged anadromous Dolly Varden ( Salvelinus malma ) by a marine mammal during summer in the Beaufort Sea based on abrupt changes in temperature and vertical movements. This observation provides insight on predator avoidance behaviour by Dolly Varden and the predator’s feeding frequency while the tag was ingested. Based on published distribution and ecology information, we presumed the predator was a beluga whale ( Delphinapterus leucas ). Supplemental satellite telemetry data from previously tagged Dolly Varden and beluga whales were used to determine the extent of spatial and vertical overlap between species in the area where predation occurred. Results Prior to the predation event, depths and temperatures occupied by the tagged Dolly Varden averaged 1.1 m and 3.1 °C, respectively. On July 7, 2020, depths remained shallow apart from a sudden dive to 12.5 m (16:45 UTC) followed by a precipitous increase in temperature from 4.4 to 27.1 °C (16:52 UTC) suggesting predation by an endotherm. Subsequent readings indicated the endotherm had a resting stomach temperature of 36.1 °C. Including the predation event, eight separate feeding events were inferred during the 20-h period the tag was ingested (before presumed regurgitation) based on subsequent declines in stomach temperatures (mean decline to 31.1 °C) that took an average of 24.1 min to return to resting temperature. The predator occupied mainly shallow depths (mean = 2.3 m), overlapping with tagged belugas that spent 76.9% of their time occupying waters ≤ 2.5 m when frequenting the area occupied by tagged Dolly Varden in the Canadian Beaufort Sea in July. Back-calculation based on tag drift and mean displacement by tagged belugas indicated the predation likely occurred west of the Mackenzie Delta. Conclusion Our findings provide new information on both anti-predator behaviour by, and marine predators of, Dolly Varden in the Beaufort Sea. We provide the first estimate of feeding frequency and stomach temperature recovery in a presumed wild beluga, and evidence for shallow foraging behaviour by belugas. Elucidating the likely predator and exploring the extent of overlap between Dolly Varden and beluga whales contributes towards knowledge on the trophic interactions in the Beaufort Sea.

The fox who cried wolf: A keywords and literature trend analysis on the phenomenon of mesopredator release

Article

Oct 2021
ECOL COMPLEX

Human activities severely impact the distribution and behaviour of apex predators in numerous terrestrial and aquatic ecosystems, with cascading effects on several species. Mesopredator outbreaks attributable to the removal of an apex predator have often been recorded and described in the literature as “mesopredator release”. During recent decades several examples of the phenomenon have been observed and studied in many different parts of the world. In this paper, we quantitatively reviewed the existing literature on mesopredator release using two software packages (VOSviewer and CiteSpace) to investigate patterns and trends in author keywords through occurrences and temporal analyses, and creating relative network maps. The results showed that even though the general scientific interest in mesopredator release has increased in recent decades, the vast majority of studies focus on canid species, leaving many other species or entire taxa (e.g., reptiles) understudied and under-described. The connection between invasive species and mesopredator release has only recently been more extensively explored and also the effects of apex predators declining in aquatic ecosystems are still only partially investigated. Due to the increasing effect of biological invasions, overfishing, and either the decline or the rise of apex predators in different parts of the world, we expect an even higher increase in interest and number of published documents on the subject. We also encourage widening the research focus beyond canids to include other important taxa.

Regional-scale variability in the movement ecology of marine fishes revealed by an integrative acoustic tracking network

Article

Full-text available

Apr 2021

Marine fish movement plays a critical role in ecosystem functioning and is increasingly studied with acoustic telemetry. Traditionally, this research has focused on single species and small spatial scales. However, integrated tracking networks, such as the Integrated Tracking of Aquatic Animals in the Gulf of Mexico (iTAG) network, are building the capacity to monitor multiple species over larger spatial scales. We conducted a synthesis of passive acoustic monitoring data for 29 species (889 transmitters), ranging from large top predators to small consumers, monitored along the west coast of Florida, USA, over 3 yr (2016−2018). Space use was highly variable, with some groups using all monitored areas and others using only the area where they were tagged. The most extensive space use was found for Atlantic tarpon Megalops atlanticus and bull sharks Carcharhinus leucas. Individual detection patterns clustered into 4 groups, ranging from occasionally detected long-distance movers to frequently detected juvenile or adult residents. Synchronized, alongshore, long-distance movements were found for Atlantic tarpon, cobia Rachycentron canadum, and several elasmobranch species. These movements were predominantly northbound in spring and southbound in fall. Detections of top predators were highest in summer, except for nearshore Tampa Bay where the most detections occurred in fall, coinciding with large red drum Sciaenops ocellatus spawning aggregations. We discuss the future of collaborative telemetry research, including current limitations and potential solutions to maximize its impact for understanding movement ecology, conducting ecosystem monitoring, and supporting fisheries management.

Are stable isotope ratios suitable for describing niche partitioning and individual specialization?

Article

Full-text available

Jul 2021
ECOL APPL

As concerns about anthropogenic and natural disturbance grow, understanding animal resource use patterns has been increasingly prioritized to predict how changes in environmental conditions, food web structure, and population dynamics will affect biological resilience. Among the tools used to assess resource use, stable isotope analysis has proliferated in ecological studies, particularly in relation to describing intra‐ and interspecific variation in trophic interactions. Despite a growing need to disseminate scientific information, the inherent limitations of stable isotope ratios and inappropriate synonymizing of distinct evolutionary and ecological processes may mislead ecological inferences in natural systems. This situation necessitates a re‐evaluation of the utility of stable isotope ratios to address certain ecological questions. Here, we assess the efficacy of stable isotope ratios to describe two fundamental ecological processes, niche partitioning and individual specialization. Investigation of these processes has increased substantially in accordance with increased access to stable isotope data. This article discusses the circumstances and approaches that are necessary to evaluate niche partitioning and individual specialization, and outlines key considerations for the associated application of stable isotope ratios.

Spatial Connectivity and Drivers of Shark Habitat Use Within a Large Marine Protected Area in the Caribbean, The Bahamas Shark Sanctuary

Article

Full-text available

Jan 2021

Marine protected areas (MPAs) have emerged as potentially important conservation tools for the conservation of biodiversity and mitigation of climate impacts. Among MPAs, a large percentage has been created with the implicit goal of protecting shark populations, including 17 shark sanctuaries which fully protect sharks throughout their jurisdiction. The Commonwealth of the Bahamas represents a long-term MPA for sharks, following the banning of commercial longlining in 1993 and subsequent designation as a shark sanctuary in 2011. Little is known, however, about the long-term behavior and space use of sharks within this protected area, particularly among reef-associated sharks for which the sanctuary presumably offers the most benefit. We used acoustic telemetry to advance our understanding of the ecology of such sharks, namely Caribbean reef sharks (Carcharhinus perezi) and tiger sharks (Galeocerdo cuvier), over two discrete islands (New Providence and Great Exuma) varying in human activity level, over 2 years. We evaluated which factors influenced the likelihood of detection of individuals, analyzed patterns of movement and occurrence, and identified variability in habitat selection among species and regions, using a dataset of 23 Caribbean reef sharks and 15 tiger sharks which were passively monitored in two arrays with a combined total of 13 acoustic receivers. Caribbean reef sharks had lower detection probabilities than tiger sharks, and exhibited relatively low habitat connectivity and high residency, while tiger sharks demonstrated wider roaming behavior across much greater space. Tiger sharks were associated with shallow seagrass habitats where available, but frequently transited between and connected different habitat types. Our data support the notion that large MPAs afford greater degrees of protection for highly resident species such as Caribbean reef sharks, yet still may provide substantial benefits for more migratory species such as tiger sharks. We discuss these findings within the context of species-habitat linkages, ecosystem services, and the establishment of future MPAs.

Regional-scale variability in the movement ecology of marine fishes revealed by an integrative acoustic tracking network

Article

Mar 2021

Marine fish movement plays a critical role in ecosystem functioning and is increasingly studied with acoustic telemetry. Traditionally, this research has focused on single species and small spatial scales. However, integrated tracking networks, such as the Integrated Tracking of Aquatic Animals in the Gulf of Mexico (iTAG) network, are building the capacity to monitor multiple species over larger spatial scales. We conducted a synthesis of passive acoustic monitoring data for 29 species (889 transmitters), ranging from large top predators to small consumers, monitored along the west coast of Florida, USA, over 3 yr (2016-2018). Space use was highly variable, with some groups using all monitored areas and others using only the area where they were tagged. The most extensive space use was found for Atlantic tarpon Megalops atlanticus and bull sharks Carcharhinus leucas . Individual detection patterns clustered into 4 groups, ranging from occasionally detected long-distance movers to frequently detected juvenile or adult residents. Synchronized, alongshore, long-distance movements were found for Atlantic tarpon, cobia Rachycentron canadum , and several elasmobranch species. These movements were predominantly northbound in spring and southbound in fall. Detections of top predators were highest in summer, except for nearshore Tampa Bay where the most detections occurred in fall, coinciding with large red drum Sciaenops ocellatus spawning aggregations. We discuss the future of collaborative telemetry research, including current limitations and potential solutions to maximize its impact for understanding movement ecology, conducting ecosystem monitoring, and supporting fisheries management.

Predators Shape Sedimentary Organic Carbon Storage in a Coral Reef Ecosystem

Article

Full-text available

Aug 2018

Trophic cascade theory predicts that predator effects should extend to influence carbon cycling in ecosystems. Yet, there has been little empirical evidence in natural ecosystems to support this hypothesis. Here, we use a naturally-occurring trophic cascade to provide evidence that predators help protect sedimentary organic carbon stocks in coral reef ecosystems. Our results show that predation risk altered the behavior of herbivorous fish, whereby it constrained grazing to areas close to the refuge of the patch reefs. Macroalgae growing in “riskier” areas further away from the reef were released from grazing pressure, which subsequently promoted carbon accumulation in the sediments underlying the macroalgal beds. Here we found that carbon stocks furthest away from the reef edge were ~24% higher than stocks closest to the reef. Our results indicate that predators and herbivores play an important role in structuring carbon dynamics in a natural marine ecosystem, highlighting the need to conserve natural predator-prey dynamics to help maintain the crucial role of marine sediments in sequestering carbon.

Activity seascapes highlight central place foraging strategies in marine predators that never stop swimming

Article

Full-text available

Jun 2018

Background: Central place foragers (CPF) rest within a central place, and theory predicts that distance of patches from this central place sets the outer limits of the foraging arena. Many marine ectothermic predators behave like CPF animals, but never stop swimming, suggesting that predators will incur 'travelling' costs while resting. Currently, it is unknown how these CPF predators behave or how modulation of behavior contributes to daily energy budgets. We combine acoustic telemetry, multi-sensor loggers, and hidden Markov models (HMMs) to generate 'activity seascapes', which combine space use with patterns of activity, for reef sharks (blacktip reef and grey reef sharks) at an unfished Pacific atoll. Results: Sharks of both species occupied a central place during the day within deeper, cooler water where they were less active, and became more active over a larger area at night in shallower water. However, video cameras on two grey reef sharks revealed foraging attempts/success occurring throughout the day, and that multiple sharks were refuging in common areas. A simple bioenergetics model for grey reef sharks predicted that diel changes in energy expenditure are primarily driven by changes in swim speed and not body temperature. Conclusions: We provide a new method for simultaneously visualizing diel space use and behavior in marine predators, which does not require the simultaneous measure of both from each animal. We show that blacktip and grey reef sharks behave as CPFs, with diel changes in activity, horizontal and vertical space use. However, aspects of their foraging behavior may differ from other predictions of traditional CPF models. In particular, for species that never stop swimming, patch foraging times may be unrelated to patch travel distance.

The control of risk hypothesis: Reactive vs. proactive antipredator responses and stress-mediated vs. food-mediated costs of response

Article

Full-text available

Feb 2018

Scott Creel

Inducible defences against predators evolve because they reduce the rate of direct predation, but this benefit is offset by the cost (if any) of defence. If antipredator responses carry costs, the effect of predators on their prey is partitioned into two components, direct killing and risk effects. There is considerable uncertainty about the strength of risk effects, the factors that affect their strength, and the mechanisms that underlie them. In some cases, antipredator responses are associated with a glucocorticoid stress response, and in other cases they are associated with trade‐offs between food and safety, but there is no general theory to explain this variation. Here, I develop the control of risk (COR) hypothesis, predicting that proactive responses to predictable and controllable aspects of risk will generally have food‐mediated costs, while reactive responses to unpredictable or uncontrollable aspects of predation risk will generally have stress‐mediated costs. The hypothesis is grounded in laboratory studies of neuroendocrine stressors and field studies of food‐safety trade‐offs. Strong tests of the COR hypothesis will require more studies of responses to natural variation in predation risk and the physiological consequences of these responses, but its explanatory power can be illustrated with existing case studies.

The trophic ecology of Caribbean reef sharks (Carcharhinus perezi) relative to other large teleost predators on an isolated coral atoll

Article

Full-text available

Mar 2018
MAR BIOL

Bulk stable isotope analysis was used to assess the trophic level and foraging habitats of Caribbean reef sharks (Carcharhinus perezi) compared to three large sympatric predatory teleosts (the Nassau grouper Epinephelus striatus, black grouper Mycteroperca bonaci, and great barracuda Sphyraena barracuda) in an isolated Caribbean coral reef ecosystem. Models and empirical studies have suggested that the depletion of large-bodied sharks in coral reef ecosystems triggers a trophic cascade that could affect the benthic community, favoring algae over coral. The hypothesized cascade is based on the premise that sharks prey on large piscivorous teleost fish that in turn prey on key herbivorous fish. Analysis of nitrogen-stable isotopes (δ15N) from white muscle tissue revealed neither adult or juvenile Caribbean reef sharks were significantly enriched in 15N compared with sympatric predatory teleost species. Linear regression found no evidence of an ontogenetic increase in nitrogen with increasing body size for Caribbean reef sharks; however, there was a significant positive relationship between body size and carbon isotope (δ13C) values. These results suggest that Caribbean reef sharks in isolated systems do not act as the apex predator in coral reef ecosystems primarily feeding on large-bodied sympatric teleosts. Instead, Caribbean reef sharks form part of an upper trophic-level predator guild alongside large-bodied teleosts, which makes the predicted trophic cascade as a result of the removal of reef sharks unlikely. Moreover, the body size–δ13C relationship suggests Caribbean reef sharks exhibit ontogenetic and individual variation in where they feed. The ecological role of this species is, therefore, complex and contextual, similar to carcharhinid species in the Indo-Pacific, emphasizing the need to further elucidate the interactions between reef sharks and the overall coral reef ecosystem so as to best inform effective conservation and management of the species.

Physiological stress responses to natural variation in predation risk: evidence from white sharks and seals

Article

Full-text available

Dec 2017
ECOLOGY

Predators can impact ecosystems through consumptive or risk effects on prey. Physiologically, risk effects can be mediated by energetic mechanisms or stress responses. The predation-stress hypothesis predicts that risk induces stress in prey, which can affect survival and reproduction. However, empirical support for this hypothesis is both mixed and limited, and the conditions that cause predation risk to induce stress responses in some cases, but not others, remain unclear. Unusually clear-cut variation in exposure of Cape fur seals (Arctocephalus pusillus pusillus) to predation risk from white sharks (Carcharodon carcharias) in the waters of Southwestern Africa provides an opportunity to test the predation-stress hypothesis in the wild. Here, we measured fecal glucocorticoid concentrations (fGCM) from Cape fur seals at six discrete islands colonies exposed to spatiotemporal variation in predation risk from white sharks over a period of three years. We found highly elevated fGCM concentrations in seals at colonies exposed to high levels of unpredictable and relatively uncontrollable risk of shark attack, but not at colonies where seals were either not exposed to shark predation or could proactively mitigate their risk through antipredatory behavior. Differences in measured fGCM levels were consistent with patterns of risk at the site and seasonal level, for both seal adults and juveniles. Seal fGCM levels were not correlated with colony population size, density, and geographic location. Investigation at a high risk site (False Bay) also revealed strong correlations between fGCM levels and temporal variation in shark attack rates, but not with shark relative abundance. Our results suggest that predation risk will induce a stress response when risk cannot be predicted and/or proactively mitigated by behavioral responses.

Ecosystem Function and Services of Aquatic Predators in the Anthropocene

Article

Mar 2019
TRENDS ECOL EVOL

Arguments for the need to conserve aquatic predator (AP) populations often focus on the ecological and socioeconomic roles they play. Here, we summarize the diverse ecosystem functions and services connected to APs, including regulating food webs, cycling nutrients, engineering habitats, transmitting diseases/parasites, mediating ecological invasions, affecting climate, supporting fisheries, generating tourism, and providing bioinspiration. In some cases, human-driven declines and increases in AP populations have altered these ecosystem functions and services. We present a social ecological framework for supporting adaptive management decisions involving APs in response to social and environmental change. We also identify outstanding questions to guide future research on the ecological functions and ecosystem services of APs in a changing world.

Landscapes of Fear: Spatial Patterns of Risk Perception and Response

Article

Feb 2019
TRENDS ECOL EVOL

Animals experience varying levels of predation risk as they navigate heterogeneous landscapes, and behavioral responses to perceived risk can structure ecosystems. The concept of the landscape of fear has recently become central to describing this spatial variation in risk, perception, and response. We present a framework linking the landscape of fear, defined as spatial variation in prey perception of risk, to the underlying physical landscape and predation risk, and to resulting patterns of prey distribution and antipredator behavior. By disambiguating the mechanisms through which prey perceive risk and incorporate fear into decision making, we can better quantify the nonlinear relationship between risk and response and evaluate the relative importance of the landscape of fear across taxa and ecosystems.

Evidence for rapid recovery of shark populations within a coral reef marine protected area

Article

Apr 2018
BIOL CONSERV

There is limited evidence on the rate at which the shark populations of coral reefs can rebound from over-exploitation, the baselines that might signify when recovery has occurred and the role of no-take Marine Protected Areas (MPA) in aiding this process. We surveyed shark assemblages at Ashmore Reef in Western Australia using baited remote underwater video stations in 2004 prior to enforcement of MPA status and then again in 2016 after eight years of strict enforcement. We found an increase in the relative mean abundance of Carcharhinus amblyrhynchos from 0.16 ± 0.06 individuals h−1 in 2004 to 0.74 ± 0.11 individuals h−1 in 2016, a change that was also accompanied by a shift in the assemblage of sharks to greater proportions of apex species (from 7.1% to 11.9%) and reef sharks (from 28.6% to 57.6%), and a decrease in the proportional abundance of lower trophic level species (from 64.3% to 30.5%). Abundances and trophic assemblage of sharks at Ashmore Reef in 2004 resembled those of the Scott Reefs, where targeted fishing for sharks still occurs, whereas in 2016, abundances and trophic structures had recovered to resemble those of the Rowley Shoals, a reef system that has been a strictly enforced MPA for over 25 years. The shift in abundance and community structure coincident with strict enforcement of the MPA at Ashmore Reef has occurred at a rate greater than predicted by demographic models, implying the action of compensatory processes in recovery. Our study shows that shark communities can recover rapidly after exploitation in a well-managed no-take MPA.

Predator declines and morphological changes in prey: Evidence from coral reefs depleted of sharks

Article

Jan 2018

Evidence from the wild as to the ecological and evolutionary consequences of top predator depletions remains limited, especially in marine systems. Given the pace and extent of predator loss, an understanding of these processes is important. Two sets of adjacent coral reef systems off north-western Australia have similar biological, physical and environmental conditions, but one of the reef systems has been exposed to nearly exclusive commercial fishing of sharks. Across reefs where sharks have been depleted, prey fishes had significantly smaller caudal fins and eyes compared to the reefs with intact shark populations (up to 40 and 46% relative difference in standardized means). These patterns were consistent across 7 teleost prey species (N = 611 individuals) that vary in behavior, diet and trophic guild. We hypothesize that these morphological patterns were primarily driven by differences in shark predation. Morphological differences were not consistent with plausible alternative explanations (habitat complexity, temperature, light, current, food availability, prey targets, competition) as primary drivers. These results provide field evidence of morphological changes in prey potentially due to predator depletions consistent with ecological predictions; specifically, predator loss caused a reduction in the size of prey morphological traits associated with predator detection and evasion. While our analysis cannot differentiate between rapid evolutionary change versus morphological plasticity due to shark depletions, either possible outcome would indicate that predator removals may have profound effects on body shapes of prey communities. This is particularly significant in the case of sharks, given that the consequences of their widespread removal have been a topic of significant speculation, debate and concern.

Trophic cascades and the transient keystone concept

Article

Aug 2017
BIOL CONSERV

Apex predator reintroductions are commonly motivated by the imperative to restore populations and wider ecosystem function by precipitating trophic cascades that release basal species. Yet evidence for the existence of such cascades is often equivocal, particularly where consumptive interactions between apex and intermediate predators are weak or absent. Here, using a tri-trophic skate-crab-bivalve study-system, we find that non-consumptive interactions between apex skate and intermediate crabs cascade down to consumptive interactions between crabs and bivalves, significantly reducing bivalve mortality. However, skate only functioned as keystone where crabs foraged for bivalves in the absence of mature bivalve reef: where reef was present, bivalve mortality was not significantly different in the presence or absence of skate. By facilitating the establishment of basal species which, in turn, diminish apex-intermediate effects, the skate's keystone function is subject to negative regulation. Thus, we propose that keystone functionality can be transient with respect to environmental context. Our findings have two central implications for apex predator reintroductions and basic ecology: (i) species hitherto not considered as keystone may have the capacity to act as such transiently, and; (ii) keystones are known to regulate ecosystems, but transience implies that ecosystems can regulate keystone function.