10.5061/DRYAD.JWSTQJQ9R
Hammerschlag, Neil
University of Miami
Fallows, Chris
Apex Shark Expeditions
Meyer, Michael
South Africa Department of Forestry, Fisheries and the Environment
Seakamela, Simon
South Africa Department of Forestry, Fisheries and the Environment
Orndorff, Samantha
University of Miami
Kirkman, Stephen
Nelson Mandela University
Kotze, Deon
South Africa Department of Forestry, Fisheries and the Environment
Creel, Scott
Montana State University
Loss of an apex predator in the wild induces physiological changes in prey
Dryad
dataset
2021
predation risk
Predation release
Predation stress
apex predator
2022-01-12T00:00:00Z
2022-01-12T00:00:00Z
en
20184 bytes
7
CC0 1.0 Universal (CC0 1.0) Public Domain Dedication
Predators can impact prey via predation or risk effects, which can
initiate trophic cascades. Given widespread population declines of apex
predators, understanding and predicting the associated ecological
consequences is a priority. When predation risk is relatively
unpredictable or uncontrollable by prey, the loss of predators is
hypothesized to release prey from stress; however, there are few tests of
this hypothesis in the wild. A well-studied predator-prey system between
white sharks (Carcharodon carcharias) and Cape fur seals (Arctocephalus
pusillus pusillus) in False Bay, South Africa has previously demonstrated
elevated fecal glucocorticoid metabolite concentrations (fGCM) in seals
exposed to high levels of predation risk from white sharks. A recent
decline and disappearance of white sharks from the system has coincided
with a pronounced decrease in seal fGCM concentrations. Seals have
concurrently been rafting farther from shore and over deeper water, a
behavior that would have previously rendered them vulnerable to attack.
These results show rapid physiological and behavioral responses by seals
to release from predation stress. To our knowledge, this represents the
first demonstration in the wild of physiological changes in prey from
predator decline, and such responses are likely to increase given the
scale and pace of apex predator declines globally.
Boat-based surveys Between 2000 and 2020, white shark relative abundance
and predatory activity during winter months at Seal Island were monitored
daily from standardized boat-based observation surveys (as described in
Hammerschlag et al. 2017; see electronic supplementary material). Water
temperatures (°C) were recorded using the vessel’s onboard temperature
sensor and the following environmental variables were estimated:
percentage cloud cover, wind speed (kt) and direction, swell height (m),
and water visibility (m). Additionally, the relative distances of rafting
seal groups off the Island’s perimeter were estimated according to one of
three distance categories: (1) seals rafting < 5 m from the Island;
(2) seals rafting > 5 and < 10 m from the Island; and (3)
seals rafting > 10 m from the Island perimeter. Between 07:00 and
09:30 h, instances of predation by white sharks on Cape fur seals were
recorded following the approach outlined in Fallows et al. 2016 (see
electronic supplementary material). The duration of each observational
period along with the number of predatory attacks by sharks on seals
during this period were recorded to calculate white shark predation rates
(i.e. number of predation events per hour). After 09:30 h, the vessel
anchored and conducted standardized boat-based baited surveys of white
sharks following the approach described in Hammerschlag et al. 2019 (see
electronic supplementary material). Between 10:00 and 12:00 h, sharks were
attracted to the boat using a large tuna head and a seal decoy. Individual
sharks were identified based on a combination of unique scarring,
presence/absence of claspers, and individual variation in pigmentation
patterns. The duration of each baited survey was recorded, along with the
number of individuals observed. The number of different individual sharks
observed per hour during these baited surveys were calculated as a metric
of relative white shark abundance. Seal fecal sample collection and
immunoassay Seal fecal samples were collected from Seal Island during 2014
and 2015 prior to the onset of shark decline (results published in
Hammerschlag et al. 2017) and during the decline and eventual
disappearance of white sharks from the study site in 2016, 2017, and 2019.
To enable scats of different individuals, ~20 g of sample was collected
from clearly distinct defecation piles. Each sample was placed in 50 ml
screw-lid vials and frozen within 1-2 hours of collection, which occurred
between sunrise and noon. Steroid hormone metabolites were extracted from
fecal samples by drying the scat and boiling a known mass of dry feces in
ethanol following Creel et al. 2009. Glucocorticoid metabolite
concentrations in fecal extracts (fGCM) were analyzed as detailed in
Hammerschlag et al. 2017 and measured using an enzyme-linked immunoassay
with a cortisol antibody (Enzo Life Sciences ADI-900-071; see electronic
supplementary material for details on procedural validation). We expressed
fGCM concentrations as nanograms of cortisol immunoreactivity per gram of
dry feces. Statistical analysis Previous analyses applied to annual trends
in white shark relative abundance data at the study site, collected
between 2000 and 2018, revealed a significant change point in 2015, after
which (2016 onwards) white shark relative abundance began to precipitously
decline (Hammerschlag et al. 2019). Therefore, we classified the period
prior to shark decline as the years 2000 to 2015 and the post-decline
period as years 2016 through 2020. To examine annual trends in white shark
relative abundance and predation rates across the 2000–2020 time-series,
we calculated the mean number of white sharks sighted per hour and the
mean number of shark predations per hour, for each year, following the
approach of Hammerschlag et al. 2019. To compare changes in seal behavior
in relation to white shark relative abundance and predatory activity, we
evaluated annual trends in seal rafting distance from the Island by
calculating the mean daily rafting category for each year. To compare seal
stress responses to annual trends in white shark relative abundance and
predatory activity, we calculated mean fGCM concentrations by sampling
year and by period (pre-decline versus post-decline of white sharks).
Previous laboratory studies that have subjected sea lions (Eumetopias
jubatus) to an adrenocorticotropic hormone (ACTH) challenge found a lag of
up to 4 d between ACTH injection and peak fGCM (Hunt et al. 2004).
Accordingly, here we considered that measured fGCM values reflected
hormone values in seals based on stress experienced within the week prior.
Indeed, Hammerschlag et al. 2017 found a very strong correlation between
seal fGCM concentrations and mean predation rates (attacks/h) measured
within the week prior to scat collections. Accordingly, here we used
Spearman Correlation to test for a correlation between weekly shark attack
rates and associated fGCM concentrations spanning the pre- and post-
decline period. We also separately tested for correlations of seal fGCM
levels against water temperature, wind speed, swell height, water
visibility, and cloud cover. As in our analysis of the correlation between
fGCM with predation rates, we used mean values of the environmental
variables recorded during the previous week and up to the day of scat
sampling in this analysis. Because white sharks only actively prey on
seals at Seal Island during winter months, we restricted analyses to data
collected from May through September, such that all data reflected seal
behavior and physiology during the season in which seals historically
experienced high predation risk. All statistical analyses were performed
in SAS with P < 0.05 used as a threshold for strong evidence of an
effect.
The files 'Shark_Sightings_MaytoSept_summarized.csv',
'Predations_MaytoSept_summarized.csv', and
'Seal_Rafting_MaytoSept_summarized.csv' were all used to create
Figure 1A, 1B, and 1C, respectively in the manuscript. The file
'fGCM_samples_raw_data.csv' was used to create Figure 2A in the
manuscript, and the file
"GW_Predations_7days_priorto_FGCM_collections_Environmental
data.csv' was used to create Figure 2B.