Same species, different prerequisites: investigating body condition and foraging success in young reef sharks between an atoll and an island system

Abstract

Abstract Acquiring and storing energy is vital to sharks of all age-classes. Viviparous shark embryos receive endogenous maternal energy reserves to sustain the first weeks after birth. Then, in order to maintain body condition, sharks must start foraging. Our goal was to understand whether maternal energy investments vary between blacktip reef sharks (Carcharhinus melanopterus) from two populations and to what extent body condition and the initiation of foraging might be affected by presumably variable maternal investments. A total of 546 young sharks were captured at St. Joseph atoll (Seychelles) and Moorea (French Polynesia) between 2014 and 2018, and indices of body condition and percentage of stomachs containing prey were measured. Maternal investment was found to be site-specific, with significantly larger, heavier, and better conditioned individuals in Moorea. Despite these advantages, as time progressed, Moorea sharks exhibited significant decreases in body condition and were slower to initiate foraging. We suggest that the young sharks’ foraging success is independent of the quality of maternal energy resources, and that other factors, such as prey availability, prey quality, and/or anthropogenic stressors are likely responsible for the observed differences across sites. Insights into intraspecific variations in early life-stages may further support site-specific management strategies for young sharks from nearshore habitats.

Full text

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Same species, dierent
prerequisites: investigating body
condition and foraging success in
young reef sharks between an atoll
and an island system
Ornella C. Weideli
1,2, Ian A. Bouyoucos1,3, Yannis P. Papastamatiou4, Gauthier Mescam5,
Jodie L. Rummer3 & Serge Planes1,6
Acquiring and storing energy is vital to sharks of all age-classes. Viviparous shark embryos receive
endogenous maternal energy reserves to sustain the rst weeks after birth. Then, in order to maintain
body condition, sharks must start foraging. Our goal was to understand whether maternal energy
investments vary between blacktip reef sharks (Carcharhinus melanopterus) from two populations and
to what extent body condition and the initiation of foraging might be aected by presumably variable
maternal investments. A total of 546 young sharks were captured at St. Joseph atoll (Seychelles) and
Moorea (French Polynesia) between 2014 and 2018, and indices of body condition and percentage of
stomachs containing prey were measured. Maternal investment was found to be site-specic, with
signicantly larger, heavier, and better conditioned individuals in Moorea. Despite these advantages,
as time progressed, Moorea sharks exhibited signicant decreases in body condition and were slower
to initiate foraging. We suggest that the young sharks’ foraging success is independent of the quality
of maternal energy resources, and that other factors, such as prey availability, prey quality, and/or
anthropogenic stressors are likely responsible for the observed dierences across sites. Insights into
intraspecic variations in early life-stages may further support site-specic management strategies for
young sharks from nearshore habitats.
Acquiring and storing energy reserves to maintain body functions and survival is vital to animals of all
age-classes1. To estimate energy reserves during various life-stages, body condition, as a proxy of animal health,
is commonly used2, with animals in good body condition presumably associated with relatively larger energy
reserves2,3. At birth, an animal’s body condition is determined by the parents, notably by the mother4. Depending
on maternal size and age at parturition, the diet, as well as the environmental conditions to which the mother was
exposed during gestation, the ospring’s size, body mass, and body condition can vary among and within species.
Indeed, coral reef shes from high quality habitats pass on larger yolk reserves to their ospring than parents liv-
ing in low quality habitats5. In the rst weeks aer birth, young animals with no parental care are required to grad-
ually incorporate autonomous foraging activities to their daily routine to sustain their energy reserves. Hence,
young animals depend on prey resources and habitat quality, in addition to remaining maternal energy resources.
While strong positive relationships between parental energy reserves and factors such as ospring condition and
time to exogenous feeding have been noted for teleost shes and marine reptiles5–8, little work has been done on
1PSL Research University: EPHE-UPVD-CNRS, USR 3278 CRIOBE, 66860, Perpignan, France. 2SOSF - D’Arros
Research Centre (SOSF-DRC), c/o Save Our Seas Foundation (SOSF), CH-1201, Geneva, Switzerland. 3Australian
Research Council Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Queensland, 4811,
Australia. 4Department of Biological Sciences, Marine Sciences Program, Florida International University, North
Miami, Florida, 33181, USA. 5Projects Abroad, Shark Conservation Project Fiji, West Sussex, BN124TX, United
Kingdom. 6Laboratorie d’Excellence ‘CORAIL’, EPHE, PSL Research University, UPVD, CNRS, USR 3278 CRIOBE,
Papetoai, Moorea, French Polynesia. Correspondence and requests for materials should be addressed to O.C.W.
(email: ornella.weideli@gmail.com)
Received: 17 May 2019
Accepted: 27 August 2019
Published: xx xx xxxx
OPEN
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maternal energy investment in elasmobranchs. As maternal investment may vary with life-history traits (e.g., size,
body condition) and habitat, it is also important to understand if and to what extent the level of maternal energy
investment aects the ospring’s condition and foraging development during the rst weeks of life.
Elasmobranchs occur across a range of heterogenous habitats and experience variable environmental condi-
tions and levels of anthropogenic threats that dierentially aect life-history traits9. While intraspecic dierences
in life-history traits may be less distinctive in sharks with broad movement patterns, genetically and geograph-
ically isolated sharks with restricted movements and site-delity are known to exhibit pronounced intraspecic
dierences in size at birth, growth rates, and litter sizes9,10. Adult reef-sharks from the family Carcharhinidae
have been the focus of a number of studies investigating such dierences10, but fewer studies have characterized
intra-specic variability among populations of young animals. Barker et al.11, for example, reported that larger
sized female lemon sharks (Negaprion brevirostris) from Florida’s Marquesas Keys (USA), give birth to larger
ospring than the smaller sized females from a nearby nursery11. Likewise, Hussey et al.12 revealed an increase in
maternal reproductive output (larger neonatal mass) with increasing maternal size in two carcharhinid sharks.
While such size and body mass measurements can help assess characteristics of young shark populations13, their
relationship (e.g., body mass per unit size) provides invaluable information on energy reserves, overall body con-
dition and tness2,3,14,15. Despite the importance of energy reserves, it is unclear as to whether maternal energy
investment varies across shark populations adopting dierent life-history traits.
At birth, viviparous sharks receive endogenous energy reserves, primarily stored as lipids in livers, from their
mothers12,16–18. Although this maternal energy allocation can lead to signicantly enlarged livers in neonatal
sharks (up to 20% of total body mass12), this endogenous energy transfer is nite. As opposed to marine mam-
mals, where exogenous maternal energy provisioning (e.g., lactation) can last months to years, depending on spe-
cies19, sharks receive no maternal aercare. is results in energy resources being utilized within the rst weeks, as
demonstrated by decreasing condition indices12,17. Similarly, Duncan and Holland16 reported mass loss in young
sharks following parturition, most likely a sign of depleted energy reserves. To counteract such declines, young
sharks are required to incorporate autonomous foraging to their daily routine. As it is dicult to directly observe
young sharks foraging in the wild, biomarkers that indirectly estimate when young sharks shi from relying on
maternal energy resources to feeding autonomously have recently been established20,21. Although biomarkers,
such as bulk stable isotopes, alone20,22 or in combination with fatty acids21, provide insights into autonomous for-
aging developments and broad estimates of body condition23,24, isotopic turnover rates impede timely and precise
estimates of body condition as well as foraging development. To date, Hussey et al.12 executed the only study that
simultaneously and precisely assessed changes in body condition and estimated foraging development in early
life-stages of sharks12 via a combination of lethal and non-lethal measurements to calculate such developments
across dierent umbilical scar healing stages. Given that the study only focused on a single location that precludes
investigations on variabilities among populations, further work is needed to understand if and how body condi-
tion and the development of autonomous foraging may vary across species inhabiting dierent habitats.
To examine intraspecic variability in body condition and foraging development during the rst weeks of
life, we collected life-history data from neonatal and juvenile blacktip reef sharks (Carcharhinus melanopterus), a
species with high levels of genetic population structure25,26, from two remote habitats in the Indo-Pacic Ocean.
While Moorea (French Polynesia) is a remote island with human-impacted shorelines in the South Pacic, St.
Joseph atoll (Seychelles), located in the western Indian Ocean, consists of a small and uninhabited ring of islands
with adjacent shallow reef ats. Our objectives were to use non-lethal methods to determine (1) whether maternal
energy investment varies between C. melanopterus populations potentially adopting dierent life-history strate-
gies, and (2) if and to what extent body condition and foraging development might be aected by presumably var-
iable maternal investments. We hypothesized that better conditioned neonates (e.g., neonates with higher energy
stores) would show a slower decrease in body condition and a faster acquisition of foraging skills during the rst
weeks of life. Considering the steady increase in human activities in nearshore areas that is resulting in declining
preyabundanceand habitats16,27,28 as well as predicted higher water temperatures due to climate change29,30, a
better understanding of maternal energy investments, body condition, and autonomous foraging development
during early life-stages of sharks has important implications for conservation31. Insights into potential intraspe-
cic dierences in such characteristics may further support site-specic management strategies for sharks from
remote and potentially prey-limited habitats32,33.
Results
Intraspecic variation in maternal energy investments. In Moorea, during the parturition seasons
in 2016/2017 and 2017/2018, a total of 313 neonatal and juvenile C. melanopterus were captured and meas-
ured. Of those, 163 individuals (52%) were categorized as neonates (based on the presence of open or semi-
healed umbilical scars) ranging from 368 to 466 mm LPC (418.42 ± 18.90 mm, Fig.1a) and weighting 670 to
1500 g (1025.22 ± 148.75 g, Fig.1b). At St. Joseph, during the parturitionseasons in 2014/2015, 2015/2016 and
2016/2017, a total of 233 neonatal and juvenile C. melanopterus were collected. Of those, 173 individuals (74%)
were categorized as neonates ranging from 287 to 459 mm LPC (372.22 ± 27.66 mm, Fig.1a) and weighting 300 to
1375 g (694.99 ± 182.71 g, Fig.1b). Neonatal C. melanopterus from Moorea were signicantly larger (two sample
t-test: t = 17.769, df = 334, p < 0.0001) and heavier at birth (two sample t-test: t = 17.917, df = 325, p < 0.0001)
than individuals from St. Joseph. Mean water temperatures during the pupping seasons were signicantly lower in
Moorea (29.5 °C ± 0.003) compared to St. Joseph (30.0 °C ± 0.003; two sample t-test: t = −101.87, df = 1040400,
p < 0.0001; see Supplementary InformationS1).
Body condition, as calculated via three methods, diered signicantly across locations. Neonatal sharks
from Moorea were heavier for any given size than those at St. Joseph (F1,234 = 20.89, p < 0.001), and length-body
mass results suggest positive allometric growth (Fig.2). Independent indices of body condition were signi-
cantly higher in Moorea sharks compared to St. Joseph sharks, as calculated by Fulton’s K (two sample t-test:
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t = 6.083, df = 535, p < 0.0001; Fig.3a) and GF (two sample t-test: t = 7.036, df = 402, p < 0.0001; Fig.3b). Linear
regressions revealed no relationships between LPC and Fulton’s K (St. Joseph: F1,222 = 2.247, p = 0.135), and LPC
and GF (Moorea: F1,311 = 1.035, p = 0.310; St. Joseph: F1,89 = 3.397, p = 0.069; see Supplementary InformationS2).
However, linear regressions revealed signicant negative relationships between LPC and Fulton’s K in Moorea
sharks (F1,311 = 11.280, r2 = 0.04, p = 0.0009; see Supplementary InformationS2).
Figure 1. Percentage frequency histogram of (a) precaudal length (LPC) and (b) total body mass (MTB) in
neonatal Carcharhinus melanopterus (USS1 and USS2) from Moorea (black, n = 163) and St. Joseph (white,
n = 173, 164 respectively).
Figure 2. Relationship between total body mass (MTB) and precaudal length (LPC) of neonatal Carcharhinus
melanopterus (USS1 and USS2) from Moorea (black, y = 0.042472x2.70, r2 = 0.69, n = 163) and St. Joseph
(y = 0.013947x2.98, r2 = 0.73, n = 164).
Figure 3. Comparison of body condition indices across locations. (a) Fulton’s K for neonataland juvenile
Carcharhinus melanopterus from Moorea (n = 313) and St. Joseph (n = 224). (b) Girth factor GF for
neonataland juvenile Carcharhinus melanopterus from Moorea (n = 313) and St. Joseph (n = 91). Boxes indicate
the interquartile range with the median shown by horizontal lines, minimum and maximum values shown by
whiskers, and points representing outliers.
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Intraspecic variation in change of body condition. In cases where body condition indices did not
conform to a normal distribution (Shapiro-Wilks test, p < 0.05), non-parametric one-way and multiple com-
parison tests were applied. Body condition, as estimated by Fulton’s K in young sharks from Moorea, diered
signicantly among increasing umbilical scars stages (ANOVA, F2,310 = 6.907, p = 0.001). Specically, pair-wise
comparisons showed statistical dierences between USS1 and USS3 (Tukey’s HSD, t = −0.06, p = 0.001) and
decreasing, albeit non-signicant, body condition between USS1 and USS2 (Tukey’s HSD, t = −0.03, p = 0.179)
and between USS2 and USS3 (Tukey’s HSD, t = −0.03, p = 0.097, Fig.4a). Body condition, as estimated by girth
factor GF in young sharks from Moorea, decreased signicantly as umbilical scar stages increased (Kruskal-Wallis
test, χ2 = 48.513, df = 2, p < 0.001). Pair-wise comparisons reported signicant dierences between all three
umbilical scar stage classes (Dunn test, USS1/USS2: p = 0.0006; USS1/USS3: p < 0.0001; USS2/USS3: p = 0.0003,
Fig.4c). On the contrary, no signicant dierences were found between Fulton’s K and GF with increasing umbil-
ical scar healing stages in young sharks from St. Joseph (Kruskal-Wallis test, χ2 = 8.6627, df = 2, p = 0.056 and
χ2 = 2.8051, df = 2, p = 0.246, respectively; Fig.4b,d).
e 45 individuals that were recaptured in Moorea during one parturition season were at liberty from 4 to
72 days (see Supplementary InformationS3), and linear regressions showed signicant negative relationships
between changes in Fulton’s K and time at liberty (F1,43 = 5.41, p = 0.025, r2 = 0.11, Fig.5a). Linear regression
further revealed decreasing, albeit non-signicant, relationships between GF and time at liberty (F1,45 = 2.75,
p = 0.104; Fig.5b). Similarly, linear regression indicated signicant negative relationships between change in
body condition with body condition at initial capture (Fulton’s K; F1,43 = 28.46, r2 = 0.40, p < 0.0001; Fig.6a; GF:
F1,43 = 31.71, r2 = 0.42, p < 0.0001, Fig .6b). When dierences in body condition indices were regressed against
one another, data showed that changes in Fulton’s K could be predicted by changes in GF (F1,43 = 16.83, r2 = 0.28,
p = 0.0002; see Supplementary InformationS4), suggesting that estimates of either condition index were consist-
ent within individuals.
Intraspecic variation in foraging success. In Moorea, over the scope of one parturition season (year
2016/2017), 165 gastric lavages in C. melanopterus resulted in 78 full (47%), and 87 empty (53%) stomachs. At St.
Joseph, over the scope of two parturition seasons (years 2015/2016 and 2016/2017), 109 gastric lavages in young
C. melanopterus provided 93 full (85%) and 16 empty (15%) stomachs, leading to a signicant bias of stomach
fullness with locations (Χ2 = 36.60, p < 0.0001). When separated by USS, the frequency of stomachs containing
prey items (increased foraging success) increased from 30% (USS1; n = 17) and 47% (USS2; n = 51) to 51% by
USS3 in Moorea (n = 97; Fig.7). At St. Joseph at USS2, 100% of sampled stomachs had prey items in them (n = 8),
and 84% of 101 individuals at USS3had stomachs containing prey (Fig.7). e smallest acrylic tubes (2.5 cm
outer diameter) were still too large to be used with the smallest individuals from St. Joseph, resulting in a lack of
sampled USS1 individuals.
Figure 4. Transition of body condition indices with increasing umbilical scar stages (USS) in Carcharhinus
melanopterus. Fulton’s K at (a) Moorea and (b) St. Joseph, and girth factor GF at (c) Moorea, and (d) St. Joseph.
Boxes indicate the interquartile range with the median shown by horizontal lines, minimum and maximum
values shown by whiskers, and black dots represent outliers. Letters above plots in (a) and (c) indicate
statistically signicant dierencesbetween groups. Sample size in Moorea: USS1 n = 59, USS2 n = 104, USS
3 n = 150. Sample size at St. Joseph: USS1 n = 2, USS2 n = 29, USS3 n = 60.
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Discussion
is study represents the rst non-lethal investigation of body condition and concurrent estimates of autono-
mous foraging development in young C. melanopterus from two isolated shark populations. Our data provide
compelling evidence that maternal investment is site-specic, with signicantly larger sizes, greater body masses,
Figure 5. Changes in body condition indices with time at liberty in Carcharhinus melanopterus from Moorea.
(a) Change in Fulton’s K over time at liberty, and (b) change in girth factor GF over time at liberty. Data were
obtained from neonatal sharks that were measured twice within the same parturition season (min. 4 days, max.
72 days, n = 45). e regression line for predicting changes in Fulton’s K from time at liberty is shown in red
(y = 0.001–0.003x, r2 = 0.11). Note that each dot represents the change of body condition in one individual and
that negative values (below the dashed line) depict a decrease of body condition in an individual shark.
Figure 6. Changes in body condition indices versus body condition indices at initial capture in neonatal
Carcharhinus melanopterus from Moorea. (a) Change in Fulton’s K versus Fulton’s K at initial capture, and (b)
change in girth factor GF versus girth factor GF at initial capture. Data were obtained from sharks that were
measured twice within the same parturition season (min. 4 days, max. 72 days, n = 45). e regression lines
are shown in red (K: y = 0.94 - 0.73x, r2 = 0.40 and GF: y = 0.90 - 0.84x, r2 = 0.42, respectively). Note that each
dot represents the change of body condition in one individual and that negative values (below the dashed line)
depict a decrease of body condition in an individual shark.
Figure 7. Frequency histogram of percentagestomachs containing preywith increasing umbilical scar stage
(USS) in Carcharhinus melanopterus from Moorea (black, n = 165) and St. Joseph (white, n = 109). Numbers
above each column represent the total sample size of sharks for a given umbilical scar stage (USS) on which
gastric lavages were performed.
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and larger body condition measurements in Moorea sharks when compared to St. Joseph sharks. Furthermore,
our data suggest that, despite this better head start, young sharks in Moorea exhibited signicant decreases in
body condition and developed foraging habits slower than sharks from St. Joseph (e.g., fewer than half of the
stomachs lavaged from sharks in Moorea had contents during later development stages). ese dierences in
foraging success likely explain the signicant decrease in body condition in Moorea sharks, while sharks at St.
Joseph maintained their body condition. Likewise, data from recaptured individuals from Moorea conrm the
signicant decrease in body condition with increasing time at liberty (up to 72 days). Recaptured individuals that
initially had higher body condition indices were most likely to exhibit declines in body condition during the rst
weeks/months of life.
e fact that we observed larger and heavier neonates with greater mass per unit length and higher condition
indices in Moorea versus St. Joseph suggests that neonates in Moorea are being well provisioned by larger, better
conditioned mothers with potentially lower fecundity. Indeed, adult C. melanopterus from Moorea tend to be
larger34 than adult C. melanopterus from St. Joseph35 and are therefore likely to produce larger, heavier and better
conditioned young12. Body size is strongly heritable, and it’s also common for geographically separated shark pop-
ulations of the same species to be genetically and morphologically dierent9,10,34. Body size, or at least body con-
dition, can further be inuenced by a species’ diet. Data on natural prey abundance were not collected in either
of the two study locations, but provisioning sites in Moorea are numerous, and adult C. melanopterus frequent
such sites36. While direct impacts of provisioning on body condition is either sparsely documented37,38 or show
minimal impacts on the sharks’ diet39, provisioned female C. melanopterus may benet from high-trophic level
food, which, in turn, is likely to augment maternal investments (e.g., more endogenous energy resources) for their
ospring. Further, the exclusive economic zone (EEZ) of French Polynesia banned shing for C. melanopterus in
200640. is shing ban may have helped protect larger and better conditioned females, which in turn give birth to
larger, heavier, and better conditioned ospring12. Lastly, it could be argued that dierences in fecundity inuence
variable pup sizes in Moorea and St. Joseph. While the estimated average litter size of sharks from Moorea and
Aldabra (~900 km southwest of St. Joseph) is three pups, Moorea’s sharks demonstrate annual reproductive cycles
as opposed to biennial cycles in Seychelles34,41,42. is suggests that, considering the very limited data, fecundity
does not explain our ndings, because more frequent cycles in Moorea would likely infer smaller pups. While any
of these mechanisms alone or in combination could explain the intraspecic variation in the level of maternal
investment of female C. melanopterus, identifying the specic factors that result in female sharks in Moorea being
larger and giving birth to larger, heavier, and better conditioned ospring was beyond the scope of this study.
e rate at which body condition and autonomous foraging success changed as umbilical scars began dis-
appearing varied between Moorea and St. Joseph sharks, suggesting early development may be site-specic for
young C. melanopterus. Although the rapid decrease of body condition in C. melanopterus from Moorea is not
surprising, considering documented declines in body conditions in other young sharks12,16,17,22, the relatively
high maternal investment in Moorea was expected to lead to slower declines in body condition (e.g., due to more
energy reserves at birth) and faster foraging development and success compared to sharks from St. Joseph. Our
study, however, demonstrates signicant declines in body condition and slower foraging development in sharks
from Moorea, therefore suggesting that the quality of the maternal energy investment is not correlated with the
foraging success of the young. Other factors, such as environmental conditions, prey resources, variable foraging
strategies, and/or anthropogenic stressors are all likely, in some part, to be responsible for the observed dier-
ences across sites.
Environmental conditions, such as seawater temperatures, were measured in Moorea and St. Joseph. Despite
signicantly lower mean temperatures during pupping seasons in Moorea (29.5 °C ± 0.003) compared to St.
Joseph (30.0 °C ± 0.003), temperature ranges were highly comparable (see Supplementary InformationS4).
ese small dierences in mean temperatures lead to standard metabolic rates (SMR; the cost of maintenance
metabolism) of 160.5 and 162.7 mg O2 kg−1 h−1, respectively (Bouyoucos, IA, unpublished data). A dierence in
SMR of 1.4% is, however, negligible in maintenance costs and is therefore likely not responsible for the observed
site-specic dierences in changes of body condition. However, if ocean temperatures continue to increase, a
decrease in body condition during early life-stages may be more pronounced, because higher water temperatures
canhave decelerating eects on growth43.
Variable rates of decreasing body condition and foraging development in young sharks may have also been
shaped by dierent levels of inter- and intraspecic competition in young sharks for limited prey resources.
Recent studies categorize nearshore areas as resource-limited, a condition that may especially be distinctive in
remote areas, where multiple juvenile shark species co-occur and compete for similar prey44–46. Both Moorea and
St. Joseph are inhabited by multiple populations of young sharks13,20, therefore, competition is likely to occur at
both locations18. Indeed, co-occurrence and potential competition in Moorea lead to isotopic niche partition-
ing between juvenile C. melanopterus andsicklen lemon sharks (Negaprion acutidens); yet, body condition as
well as growth rates were not aected by the coexisting species45. Even if prey abundances were not quantita-
tively assessed in any of the two study sites, small reef-associated teleosts (e.g., the predominant prey of young
sharks41,47) are oen observed in St. Joseph at site of collection (Weideli, OC, personal observation) and in 85%
of stomachs investigated. ese observations suggest that prey availability at St. Joseph is sucient, resulting
in potentially weak competitive interactions between young sharks. At Moorea, during gillnet deployments
(n = 175) for this study, potential prey species were rarely observed; although this does not prove their absence.
Future studies assessing competitive patterns among coexisting shark species and prey availability are, however,
needed to draw further conclusions as to why body condition and foraging development during the rst weeks of
life change at dierent rates in Moorea and St. Joseph.
In addition to prey availability, the caloric value of ingested prey as well as foraging strategies may dier
between sites. Juvenile scalloped hammerheads (Sphyrna lewini) have been reported consuming energetically
poor prey16,48, which may explain the observed decreases in body mass aer parturition16. e liver lipids that
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young sharks in Moorea receive as a maternal headstart are potentially higher in energy compared to their
ingested prey. is caloric dierence may help explain the body condition decrease as their umbilical scars begin
to disappear, similar to the loss of maternal isotopic signals observed in young bull sharks (Carcharhinus leucas)
and Atlantic sharpnose sharks (Rhizoprionodon terraenovae)22. On the contrary, small or negligible dierences in
energetic value of maternal energy resources compared to young sharks’ prey may explain the maintained body
condition observed in St. Joseph sharks. Low caloric prey may also help to explain how an increase in foraging
success from 30% and 47% to 51% of stomachscontaining prey (Fig.7) can result in decreasing body condition
in Moorea sharks. Similar ndings have been reported by Hussey et al.12, where body condition of neonatal dusky
sharks (Carcharhinus obscurus) decreased despite increasing stomach contentmass (increasing feeding activities).
Nonetheless, this is highly speculative, and more stomach items, especially those from extremely young sharks
(e.g., USS1 fresh umbilical scars), as well as the actual caloric value of the stomach contents are needed to better
understand the relationship between decreasing body condition despite increasing foraging success.
Prey resources and their caloric value may deteriorate in nearshore areas with substantial anthropogenic
impacts28,49. Indeed, the abundance of small reef-associated teleosts is declining through large-scale habitat deg-
radation27,50, and artisanal shing51. Likewise, anthropogenic habitat degradation underpins the declines in the
abundance of energetically high-value prey species (e.g., small scarids) with a concurrent increase of low caloric
gobies and shrimps in the shallow areas of Kāne’ohe Bay, Hawai’i (USA)52. is transition to lower caloric-value
prey is thought to be partially responsible for the declining body mass in S. lewini during their rst weeks of life16.
Anthropogenic stressors, however, can also have direct impacts on young sharks. Increasing temperatures and
salinity, for example, allowed young C. leucas to expand into formerly uninhabited bays53 with potentially dier-
ent prey resources and also into areas where artisanal nearshore sheries frequently capture young sharks54,55.
Even if young sharks are not the target species in artisanal sheries and are subsequently released, accidental
capture events cause stress56. Young C. melanopterus, for example, require at least 8 h recovery aer a single acci-
dental gillnet capture event; during this time, about 15% of the energy used for daily swimming is lost56. Despite
enforcement of partially protected areas (no-take zones) around Moorea57, artisanal shing is far more likely
to occur within the coastal areas of Moorea when compared to near-pristine and uninhabited St. Joseph, with
its uninterrupted reserve boundary35,40. Similarly, human activities at Moorea (e.g., boat trac, boat channel
dredging, and shoreline activities) may constrain young shark habitats, with sharks potentially avoiding deeper
channels or areas with boat trac.
e observed relationship between decreasing body condition with increasing USS in Moorea sharks is fur-
ther supported by data from individual sharks that were captured on multiple occasions. is is, to our best
knowledge, the rst evidence of a signicant decrease of body condition with time at liberty in individual wild
sharks (Fig.5). Results from such recaptures also depict that individuals with higher body condition indices
(K as well as GF) at initial capture had more pronounced decreases in body condition during the rst weeks of
life (Fig.6). is is analogous to the ndings across habitats, in which sharks from Moorea with higher mater-
nal investments were subject to signicant decreases in body condition (Fig.4a,c) compared to sharks from St.
Joseph, where such a decline was absent (Fig.4b,d). Since all recaptured individuals at Moorea were exposed to
similar environmental conditions (e.g., prey availability, prey quality, and anthropogenic stressors), other fac-
tors must have contributed to the within-population dierences around Moorea. One plausible answer could
be that sharks with higher initial body condition are less driven to start foraging because they can rely on ample
endogenous energy resources for an extended period of time. On the contrary, individuals with lower initial
body condition are forced to develop foraging skills at an earlier age, hence demonstrating a positive change in
body condition between capture events. is is speculative, because unexperienced young sharks are generally
considered as asynchronous opportunistic foragers58, and dietary information were not collected from recaptured
sharks. Also, body condition is only a proxy that may mask other behavioural or physiological traits that may have
inuenced our ndings. Future work should therefore aim to collect dietary information (e.g., stomach contents
or isotopic information) from recaptured sharks to validate changes in body condition between multiple capture
events. Finally, prospective studies are recommended to include long-term recaptures to elucidate whether the
body condition changes that are observed during early-life stages inuence later development stages or if these
early body condition changes are negligible for older age-classes.
In conclusion, our ndings suggest and support that decreases in body condition within the rst weeks of
life are common for young viviparous sharks and not only result from natural depletions of maternal energy
resources, but will also in some part be aected by prey availability, prey quality, foraging strategies, and/or
anthropogenic stressors12,16. Our approach, using two populations of C. melanopterus, further enabled us to dis-
criminate between dierent maternal investments in which young sharks from Moorea with higher maternal
energy resources were found to demonstrate signicant decreases in body condition and slower foraging develop-
ment compared to sharks from St. Joseph. A comparable observation was provided within the Moorea population
in which better-conditioned individuals were subject to a higher loss of body condition. It is therefore expected
that young sharks with relatively lower body condition are forced to develop foraging skills at an earlier life-stage,
resulting in higher proportions of stomachs containing prey and a positive change in body condition between
recaptures. is nding suggests that the habitat quality (e.g., prey abundance and quality) might be especially
important for sharks with limited maternal energy resources, and generally for sharks that occur in isolated,
nearshore habitats, where deeper surrounding waters or anthropogenically-induced channels impede or prevent
dispersal to nearby, potentially prey-rich habitats.
e continued global expansion of human activities (e.g., overshing, climate change, coastal development,
and pollution) poses the greatest risk to reef-associated, shallow water shark species59. erefore generating
site-specic information on early development of reef sharks is critical60. During these early life-stages, young
sharks not only depend on the maternal energy resources, but also rely on these nearshore areas for shelter and/
or to access adequate prey resources. erefore, to achieve sound conservation measures for C. melanopterus and
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other viviparous reef sharks, management strategies need to come together to eectively protect breeding popu-
lations as well as young sharks and theirshallow nearshore habitats.
Methods
Study location and sampling. Some of the sharks for this study were captured as part of long-term sh-
eries-independent surveys in Moorea, French Polynesia (17°30′S, 149°51′W). Moorea is surrounded by fringing
reefs and lagoons that are adjacent to shallow nearshore areas serving as putative nursery grounds for young C.
melanopterus34,45. Juvenile C. melanopterus were captured using gillnets (50.0 m × 1.5 m, 5.0 cm mesh) during the
parturition months (September – February) in 2016/2017 and 2017/2018. Captured individuals were immediately
removed from the net, and handling time was kept to a minimum (<7 min.) to avoid excessive capture-related
stress56. Sharks captured in 2016/2017 were externally tagged using coloured T-bar anchor tags (Hallprint ®,
Hindmarsh Valley, SA, Australia) and internally with passive integrated transponder (PIT) tags (Biolog-ID) in
2017/2018 to allow recaptured animals to be identied. During these sampling events, pre-caudal length (LPC, the
length from the tip of the snout to the precaudal notch) and three girth measurements were measured to the near-
est 0.1 cm with a tape measure for each shark: 1) pectoral girth (GPEC), the circumference of the shark measured
at the base of the pectoral n insertion, anterior to the dorsal n, 2) dorsal girth (GDOR), the circumference meas-
ured at the base of the rst dorsal n insertion, and 3) caudal girth (GCAU), measured anterior to the caudal n in
the precaudal notch (see Supplementary InformationS5). Umbilical scar stage (USS), a reliable indicator of neo-
natal life-stages12,16,61, was quantied into three categories. USS1 was applied if scar was fully open, USS2, if scar
was semi-healed, and USS3 for fully healed scars (see Supplementary InformationS6). Individuals with USS1 and
USS2 were considered as neonate sharks with an estimated maximal age of four weeks12,16,61. Sharks with closed
scars (USS3) were identied as young-of-the-year (>four weeks old) and no dierentiation was made between
visible and well-healed scars. We were unable to dierentiate between young-of-the-year and older sharks, due
to systematic size overlap between dierent age-classes11. e USS of each shark was photographed alongside a
ruler, and total body mass (MTB) was measured with a hand-held scale to the nearest 10 g. Aer completing basic
measurements, a subset of C. melanopterus individuals also had their stomachs ushed, similar to Bangley et al.62.
Dierent diameters of transparent acrylic tubes (2.5, 3.2, and 3.8 cm outer tube diameter) were used according to
the shark sizes (<60 cm, between 60–70 cm and >70 cm LT, respectively). e beveled and lubricated tubes were
inserted through the mouth, esophagus, and into the stomach while the sharks were kept in the water. As soon
as the stomach and the tube were lled with water, the shark was turned upside down to ush the stomach. e
stomach items were captured in a sieve, and thepercentage ofstomachs containing prey was recorded. is pro-
cedure was solely conducted on sharks in good condition (e.g., no open wounds) and was kept to a maximum of
three consecutive procedures per individual. Environmental temperatures were recorded every ten minutes dur-
ing parturition season with stationaryHobo® temperature loggers (UA-002-64, Onset Computer Corporation,
Bourne, MA, USA) deployed in capture locations.
Fieldwork was further conducted in the western Indian Ocean at St. Joseph atoll (05°26′S, 53°20′E) in the
Republic of Seychelles. St. Joseph is a near-pristine and non-inhabited atoll that oers shallow, protected areas for
at least two species of young sharks13. Juvenile C. melanopterus were captured with gillnets (20.0 m × 1.5 m, 5.0 cm
mesh) during the parturition months (October – December and March – April) in 2014/2015, 2015/2016 and
2016/2017. Captured C. melanopterus were immediately removed from the net, and handling time was kept to
a minimum (<7 min.) to avoid excessive capture-related stress56. Sharks were internally tagged using PIT tags
(Biomark®) to allow recaptured sharks to be identied. e LPC, girth, USS, and MTB were measured for each
shark, and gastric lavage was subsequently conducted using a sub-sample of sharks following Moorea’s protocol.
All sharks were released at site within minutes of capture. Temperatures were recorded every een minutes
during parturition season with stationary Hobo® temperature loggers (U22-001, Onset Computer Corporation,
Bourne, MA, USA) distributed across the area surveyed.
Data analyses. Where applicable, data were checked for normality using Shapiro-Wilk tests prior to analyses
in R version 3.5.363 within the RStudio interface ver. 1.0.15364. For all tests, the level of statistical signicance α
was set at 0.05, and results are reported as means ± SD. To investigate potential intraspecic life-history vari-
abilities in neonates and temperature dierences across habitats, mean LPC, MTB and water temperatues were
compared with two sample t-tests, and frequency histograms were subsequently constructed. Total body mass for
a given LPC was used to estimate body condition, assuming that individuals in a good condition would be heavier
than those in poorer condition of the same length. us, we determined allometric length–mass relationships by
using the formula log y = log a + b log x. ese coecients were used in MTB = a LPC b, where MTB is total body
mass (g) and LPC is length (cm).
Two independent indices of individual body condition were also calculated. e Fulton’s body condition
index, also known as Fulton’s K65, calculates a morphometric index of a sh’s body condition with the following
equation:
=
−
K10M (L )(1)
5TB PC31
We also constructed a non-lethal and morphometric condition index, based on the assumption that individu-
als with larger livers for a given body length are in better condition12. Similar to Irschick & Hammerschlag66, three
measurements along the shark’s body were chosen to incorporate the size and anatomical location of the liver, as
well as the shark’s shape, which is wider along the anterior part of the body67. While massive body sizes prevent
measuring the circumference in previous studies66,67, we were able to take three circumference measurements to
calculate the girth factor (GF) as a proxy for body condition using the following equation:
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=++−
GF [G GG]L (2)
PECDOR CAUPC1
Resulting condition indices (K and GF) were compared across locations using a two sample t-tests. To demon-
strate and validate the absence of inadvertent co-linearity between the two body condition indices and LPC2,3,
linear least-squares regressions were performed for LPC with K and GF, respectively.
In order to follow the transition of body condition with the closure of the umbilicus (increasing USS), anal-
ysis of variance (ANOVA) and Tukey’s honest signicant dierence (HSD) tests were used for post-hoc multi-
ple comparisons for Fulton’s K at Moorea. As the other comparisons did not conform to a normal distribution,
Kruskal-Wallis tests were applied. Post-hoc multiple comparisons were subsequently evaluated using Dunn tests,
while p-values were adjusted using the Holm method to reduce type I error. In addition, individual sharks from
Moorea that were captured on multiple occasions were used to further validate body condition changes during
early life stages. Recaptured individuals allowed us to calculate the change in body condition between two capture
events by subtracting body condition indices (K and GF) of the initial capture from the recapture event. Similarly,
recaptured individuals allowed us to estimate if changes in body condition depend on the body condition at
initial capture. For both calculations, values were plotted for each individual in a linear least-square regression.
Furthermore, Fulton’s K was linearly regressed against girth factor GF of recaptured C. melanopterus to demon-
strate that changes in K could be predicted by changes in GF. Finally, in order to estimate level of autonomous
foraging success during increasing USS, a sub-sample of C. melanopterus from Moorea and St. Joseph had gastric
lavages performed. e obtained stomach status (% of stomachscontaining prey) were compared with Χ2 test.
Ethical approval. Sharks for this study were captured as part of long-term sheries-independent surveys in
Moorea, French Polynesia and on St. Joseph, Republic of Seychelles. Ethical approval for Moorea was given by
James Cook University Animal Ethics Committee protocol A2089 and permission to work with sharks in French
Polynesia was obtained from the Ministère de l’Environnement (Arrete N° 9524). Research on sharks at St. Joseph
was approved by, and conducted with the knowledge of Ministry of Environment, Energy, and Climate Change,
Seychelles. Animal handling and tagging methods were conducted in accordance with the approved guidelines
of S. Planes by the Autorisation de pratiquer des expériences sur les animaux n° 006725 (1995) from the ministry
of Agriculture.
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Acknowledgements
This research was gratefully funded by the Save Our Seas Foundation (SOSF Keystone Grant 290) and the
Basler Stiung für biologische Forschung awarded to OCW. IAB was supported by a James Cook University
Postgraduate Research Scholarship. JLR was supported by an Australian Research Council (ARC) Early Career
Discovery Fellowship [PDE150101266] (2015-2017) and the L’Oréal-UNESCO Women in Science Foundation
Fellowship (2015–2016) concomitantly with an infrastructure and research allocation from the ARC Centre of
Content courtesy of Springer Nature, terms of use apply. Rights reserved

11
SCIENTIFIC REPORTS | (2019) 9:13447 | https://doi.org/10.1038/s41598-019-49761-2
www.nature.com/scientificreports
www.nature.com/scientificreports/
Excellence for Coral Reef Studies at James Cook University. e authors wish to thank the sta and volunteers
involved in this study, especially E. Jacquesson and E. Duncan at the CRIOBE, and R. Daly, C. Daly, C. Boyes, R.
von Brandis, and K. Bullock at the SOSF - D’Arros Research Centre.
Author Contributions
O.C.W. designed and coordinated the study; O.C.W., I.A.B. and J.L.R. collected eld data; O.C.W. analysed the
data and interpreted the data with Y.P.P. and I.A.B. O.C.W. wrote the manuscript with support and inputs from
I.A.B, Y.P.P., G.M., J.L.R. andS.P.; all authors gave nal approval for publication. O.C.W., I.A.B., S.P. and J.L.R.
secured the funding to support this study.
Additional Information
Supplementary information accompanies this paper at https://doi.org/10.1038/s41598-019-49761-2.
Competing Interests: e authors declare no competing interests.
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