We’ve already seen science as a muse of painting, music, sculpture, and design. In 2001, the poetic muse struck Smith College life sciences professor and clock researcher Mary E. Harrington who, smitten by the circadian rhythms of the bioluminescent algae Gonyaulax polyedra, penned a poem about these whimsical organisms. It appeared on the pages of the June 2001 issue of the Journal of Biological Rhythms and is considered the first poem to be published in a strictly scientific journal. (I discovered it through a passing mention in the excellent Internal Time: Chronotypes, Social Jet Lag, and Why You’re So Tired.)
We’ve already seen science as a muse of painting, music, sculpture, and design. In 2001, the poetic muse struck Smith College life sciences professor and clock researcher Mary E. Harrington who, smitten by the circadian rhythms of the bioluminescent algae Gonyaulax polyedra, penned a poem about these whimsical organisms. It appeared on the pages of the June 2001 issue of the Journal of Biological Rhythms and is considered the first poem to be published in a strictly scientific journal. (I discovered it through a passing mention in the excellent Internal Time: Chronotypes, Social Jet Lag, and Why You’re So Tired.)
Counterilluminating
animals use ventral photogenic organs (photophores) to mimic the
residual downwelling light and cloak their silhouette from
upward-looking predators. To cope with variable conditions of pelagic
light environments they typically adjust their luminescence intensity.
Here, we found evidence that bioluminescent sharks instead emit a
constant light output and move up and down in the water column to remain
cryptic at iso-luminance depth. We observed, across 21 globally
distributed shark species, a correlation between capture depth and the
proportion of a ventral area occupied by photophores. This information
further allowed us, using visual modelling, to provide an adaptive
explanation for shark photophore pattern diversity: in species facing
moderate predation risk from below, counterilluminating photophores were
partially co-opted for bioluminescent signalling, leading to complex
patterns. In addition to increase our understanding of pelagic
ecosystems our study emphasizes the importance of bioluminescence as a
speciation driver.
Among sharks, bioluminescence occurs in two shark families
only, the Dalatiidae (kitefin sharks) and the Etmopteridae
(lanternsharks), which are among the most enigmatic bioluminescent
organisms1, 2, 3.
Although these small deep-sea sharks encompass ~12% of current shark
diversity, with > 50 described species, their luminescence is rarely
observed. Moreover, contrary to the condition in other bioluminescent
animals, their tiny light producing organs (photophores) are primarily
controlled by hormones rather than by nerves4, 5, 6, 7 and are found in very large numbers to form a diversity of patterns whose adaptive benefit is unclear1, 8, 9, 10, 11, 12, 13. Indeed, since these organs are mostly situated on the ventral side (Fig. 1a),
counterillumination—a camouflage technique involving a ventral light
emission that cloaks the emitter's silhouette by matching the physical
characteristics of residual down-welling light14, 15—is assumed to be their main function1, 8, 16, 17. Nevertheless, counterillumination has only been experimentally demonstrated in a single coastal species, Etmopterus spinax18, and yet many bioluminescent sharks show ventral photophore-free areas (such as the ‘dark collar’ of the dalatiid Isistius brasiliensis10) and/or photophore markings on their fins, flanks and tail (in most Etmopteridae2, 11, 12, 19; Fig. 1b)
that likely perform another function. One of these photophore
aggregations, the lateral photophore marking, displays clade-specific
shapes (Fig. 1c) and its luminescence kinetics appears sexually dimorphic, which strongly supports a role in intraspecific recognition13, 20.
Figure 1: Shark photophore patterns.
Lateral spontaneous luminescence from (a) Squaliolus aliae and (b) E. spinax.
Arrows indicate photophore markings not involved in
counterillumination: Pe, pectoral; Ca, caudal; Do, dorsal; Ic,
infracaudal; La, lateral. Scale bars, 2 cm. (c) Etmopteridae lateral
photophore markings (blue color) diversity illustrated by (from left to
right): Centroscyllium ritteri, E. spinax, E. gracilispinis, E. lucifer and E. pusillus. Photographs by Mallefet. Drawings by Claes.
A recent study suggests that bioluminescence first evolved in
dalatiid sharks for counterillumination when they became part of the
pelagic fauna at the Cretaceous/Tertiary transition and that etmopterids
later adapted the initial counterilluminating pattern into a signalling
tool when they colonized deep-water niches7. Whether Dalatiidae and Etmopteridae have acquired their luminescence independently remains, however, in debate3, 7, 13, 21, 22 and the reason why some Etmopteridae such as Trigonognathus kabeyai or Etmopterus princeps lack lateral photophore markings is puzzling2, 13.
Spatial deviations from the ‘perfect’ ventral counterilluminating pattern directly affect counterillumination efficiency14.
As a consequence, complex photophore patterns (such as those with
lateral photophore markings) should only occur in species less exposed
to predation (from below) for which such deviations are more acceptable.
In the deep pelagic environment predation risk is mainly influenced by
prey detectability, which depends on the intensity of downwelling light
and thus on the depth. Quantifying predation exposure is therefore
difficult for marine pelagic species such as dalatiid and etmopterid
sharks that evolve in a three-dimensional environment, sometimes
performing daily vertical migrations8, 10, 18, 23. However, previous work on E. spinax suggested that sharks, contrary to other counterilluminating animals24, 25, 26, emit a virtually constant luminescent output and hence are isolume followers4, 18.
In that context, counterilluminating sharks would be constrained to a
particular depth during the daytime, where their ventral photophores are
iso-luminant to downwelling solar light (iso-luminance depth). Vertical
deviations from this depth would indeed make them detectable,
jeopardizing their survival27.
If confirmed, this would constitute the basis of a fixed-depth system
that allows predation risk to be investigated by visual modelling,
providing a way to test the putative link between predation pressure and
shark photophore pattern complexity.
In this study we used an innovative morpho-physiological analysis, capture data and a recent theory for pelagic vision27, 28
(i) to determine the counterilluminating capabilities of oceanic
species from both luminous shark families, (ii) to test the
isolume-following behaviour hypothesis and (iii) to propose an adaptive
explanation for the morphological diversity of shark photophore
patterns.
Counterilluminating capabilities of bioluminescent sharks
Efficient
pelagic counterilluminators must have a significant portion of their
ventral side occupied by photophores that produce a continuous light
matching the angular distribution, the wavelength and the intensity of
residual downwelling light14, 15.
Photophore density maps of the dalatiid Squaliolus aliae and the etmopterid Etmopterus splendidus, two species that respectively display the simplest and most complex photophore patterns of all sharks1, 2, 6, 7,
reveal unexpected organizational similarities. Indeed, in both species
photogenic tissue occupy > 95% of the ventral surface area and
photophore density increases centripetally from the edges to a median
area of the pattern: the maximum ventral density area, which occurs at
0.45–0.55 prepelvic length and has a width of ~0.2 interpectoral
distance (Fig. 2a; Supplementary Fig. S1).
These photophore patterns maximize downward emission of luminescence,
allowing matching to the angular distribution of residual downwelling
light. The perfect match observed for E. splendidus is achieved due to a centripetal change in photophore orientation, already observed in E. spinax29, 30.
Figure 2: Physical characteristics of shark luminescence.
(a) Photophore density maps from the dalatiid S. aliae and the etmopterid E. splendidus
(horizontal dashed lines indicate anterior and posterior wholemount
connections with adjacent low-density artefact) with associated in vivo
luminescence and transverse angular distribution (blue vectors indicate
the intensity of luminescence in selected directions). Bs, body section
at 0.5 prepelvic length. Luminous zone abbreviations same as in Fig. 1. Scale bars, 2 cm. (b) Dalatiid and etmopterid emission spectra (new data combined with published spectra18, 31) compared to published peak emission wavelength of mesopelagic coastal18 and oceanic32 waters: 1, I. brasiliensis (λmax = 455 nm); 2, S. aliae (λmax = 457 nm); 3, E. splendidus (λmax = 476 nm); 4, E. molleri (λmax = 477 nm); 5, E. spinax (λmax = 486 nm). Photographs by Mallefet. Drawings by Claes.
Spectral analysis of continuous spontaneous luminescence from five
distinct species, two dalatiids and three etmopterids, shows wavelength
peaks (λmax) falling in the bluish part of the light spectrum (Fig. 2b). While etmopterid luminescence matches closely the residual downwelling light λmax present in their environment (contrary to E. splendidus and E. molleri, E. spinax was caught in coastal green waters18), both dalatiid species emit at shorter wavelengths than expected for perfect oceanic counterillumination31, 32.
Photophore variables and iso-luminance depth
A
similar maximum ventral photophore density area appears to be present
in both simple and complex photophore patterns (see previous section of
the results). As a consequence, we used this area as a reference area to
explore differences in photophore mean diameter, photophore density and
proportion of skin surface area occupied by photophores (PAP) of 37
bioluminescent shark species (Supplementary Data 1, Supplementary Fig. S1), which encompasses ~75% of currently described photophore-bearing sharks species (Fig. 3a).
Figure 3: Shark photophore diversity.
(a) Overview of maximum ventral
photophore density (red colour on top drawing) from selected
representatives. Scale bar, 500 μm. Ce, Centroscyllium; Da, Dalatias; Eu, Euprotomicrus; Is, Isistius; Sq, Squaliolus; Tr, Trigonognathus.
Box plots and histograms of photophore mean diameter, photophore
density and PAP of 37 shark species from Etmopteridae (light green, n = 31) and Dalatiidae (dark green, n = 6) families. (b) R-square and associated P-value
for several log-log linear regressions of photophore variables
performed against capture depth. Regressions were performed either on
all species for which capture depth was available (n = 21) or on the confirmed bioluminescent species only (‘luminous’, n
= 9). (c) Log-log plot of PAP and capture depth with associated
regression line (log (capture depth) = −0.564 log (PAP) + 2.31, r2 = 0.81, P < 0.0001, n
= 21) and oceanic depth zones. Blue and green dots indicate specimens
captured in oceanic and coastal waters, respectively. Closed dots
indicate species with confirmed bioluminescent status. Unless determined
otherwise, all dots represent species of the genus Etmopterus. Photographs and drawing by Claes.
Photophore mean diameter values showed a normal distribution (mean value of 104.3 ± 4.7), ranging from ~59 μm in Squaliolus laticaudus to ~194 μm in E. spinax. Photophore density values showed a strongly left-skewed distribution (mean value of 21.2 ± 3.8 units mm−2), ranging from ~1 unit mm−2 in Centroscyllium kamoharai to ~100 units mm−2 in S. aliae. PAP values showed a slightly left-skewed distribution (mean value of 13.8 ± 1.7%), ranging from ~2% in C. kamoharai to ~56% in T. kabeyai.
To
determine if this morphological diversity leads to difference in
performance and therefore difference in iso-luminance depth, we selected
21 species to perform several log-linear regressions between photophore
variables and capture depth; results of these regressions are
summarized in Fig. 3b. The strongest relationship was found between PAP and capture depth (Fig. 3b,c),
and the slope of this relationship was not significantly different in
confirmed luminous and photophore-bearing sharks [one-way analysis of
covariance (ANCOVA), F = 0.048, P = 0.828], which supports
the idea that all species included in the regression have functional
photophores. However, this slope differed significantly (ANCOVA, F = 58.645, P
< 0.001) from the expected slope if all shark photophores were
iso-luminant i.e. had the same luminescing power for a given surface (Supplementary Fig. S2).
This suggests that shark photophores are not iso-luminant across PAP
but instead are proportionally brighter when occupying a larger
percentage of the skin (i.e. at higher PAP). In addition, the PAP−
capture depth relationship also indicates a theoretical upper depth
estimate for shark counterillumination in daytime of about 200 m, i.e.
when PAP would reach 100%.
Predation risk modelling and shark photophore pattern diversity
The
theoretical maximum predator detection distance (for a swordfish with
30 mm pupils) decreases with depth and becomes equal to target width at
~775 m, irrespective of target width (Fig. 4a). Following a recent study, this would represent the lower limit for effective counterillumination in clear oceanic waters27.
However, this value is sensitive to weather conditions and local
variations in water clarity. Predators with smaller pupils will also
have shorter detection distances (visual range). In addition, our model
reveals that the detection distance increases linearly with target width
(on a log-log scale; Fig. 4b).
Figure 4: Predation risk modelling.
(a) Relationship between upward
detection distance and target depth for two black target widths. (b)
Relationship between black target width and upward detection distance
for three mesopelagic depths (log-log plot). (c) Log-log plot of PAP and
interpectoral distance. For clarity, regression line (log (PAP) = −0.74
log (interpectoral distance) + 0.583, r2 = 0.21, P = 0.0044, n
= 37) is not shown. Axis on the right indicates occurence depth of
sharks in oceanic waters calculated from PAP using the relationship from
Fig. 3c.
Blue dashed lines represent isometric predator detection distance lines
(standardized by interpectoral distance) according to calculated
occurrence depth and interpectoral distance. These lines provide a
relative idea of the predation risk encountered by the sharks (the
higher the line value, the higher the relative risk). The one
interpectoral distance isometric line, which occurs at ~775 m (i.e. PAP
~10%) corresponds to the lower limit for efficient counterillumination.
Note that the minimum convex polygon encompassing all species with
lateral photophore markings (black symbols) only includes a single
species with no markings (grey symbols), Isistius brasiliensis.
This polygon is situated in a low-risk area (detection distance inferior
to 1000 interpectoral distance) and contains species with a minimum PAP
of ~5%. Square symbols indicate species for which mass captures by
natural predators have been recorded. Unless determined otherwise, all
dots represent species of the genus Etmopterus. Ac, Aculeola; Ce*, C. ritteri; Et* E. princeps; He, Heteroscymnoides. Other abbreviations same as in Fig. 3.
Using a log-log plot of PAP against interpectoral distance for
specimens of 37 distinct species, we found a significant negative
relationship between these two morphological variables (Fig. 4c). In this two-dimensional morphospace, species with lateral markings clearly separate from the others; only the dalatiid I. brasiliensis
is present inside the minimum convex polygon encompassing all species
with lateral markings. Using PAP as a proxy of daytime occurrence depth
(in oceanic waters, see Fig. 3c),
we superimposed relative isometric predator detection distance lines on
the graph; we show that species with complex patterns are found in a
moderate risk zone of the plot (predator detection distance ≤ 1000
interpectoral distance) and display a minimum PAP of ~5%.
Ventral shark photophores and their in vivo
luminescence appear well designed for camouflage by counterillumination.
Moreover, this camouflage technique is possibly the sole function of
dalatiid photophores since they do not form complex patterns. However,
across investigated specimens, Etmopteridae better match the residual
downwelling sunlight than Dalatiidae, thanks to a centripetal change in
photophore morphology29, 30 coupled to a tuning of luminescence wavelength, via specialized filters15 and/or alternative substrates for the light-producing reaction33, 34.
In addition to these family-related differences, shark photophores also
display an unexpected array of size, density and spatial organization.
Despite this diversity, a strong, global scaling between PAP and capture
depth is observed across sharks from the photic zone. This suggests
that sharks are isolume-followers and therefore are depth-constrained in
daytime. Yet the exact mechanism that would allow photophores to be
brighter at higher PAP remains unknown although it might be linked to
high thermal rate coefficient (Q10) for the light-producing
chemical reaction and/or the use of different light-producing molecules.
The key discovery that counterilluminating sharks follow isolumes
provides new and fundamental understanding of shark photophore
performance with major impacts on shark ecology and evolution, pelagic
ecosystem studies and by-catch management strategies.
Dalatiid and etmopterid photophores are both arranged following a centripetal density gradient, and share a similar morphology7, 8, 16, 17, 35, 36, physiological control4, 5, 6, 7, 37
and PAP–related performance. These striking similarities bring further
support to a unique evolution of luminescence in sharks and strongly
suggest that dalatiid-like counterilluminating patterns were co-opted
for bioluminescent signalling in Etmopteridae. If this is true, the
evolution towards complex photophore patterns under natural selection
must have resulted in an increase in individual fitness. But co-opting
of counterilluminating photophores for signalling involves a
reorganization of the basal counterilluminating pattern and therefore
inevitably leads to a decrease in camouflage efficiency14;
this is especially true for the lateral photophore markings that occupy
a large portion of the pattern. Complex photophore patterns would
therefore only be expected in shark species facing relaxed predation
pressure from upward-looking predators.
To the best of our
knowledge, PAP represents the first morphological estimator of a pelagic
organism's daytime occurrence depth. We suspect bioluminescent sharks'
isolume following behaviour to be a corollary of their unique
luminescence control that prevents significant changes of light
intensity within a short timeline4, 7, 38, as was already suggested18.
Other counterilluminating organisms are indeed typically able to
modulate the intensity of their luminescence by several orders of
magnitude and hence can occupy different isolumes in the water column24, 25, 26.
The PAP−capture depth relationship also suggests that bioluminescent
sharks can only inhabit the epipelagic zone (0–200 m) at night, when
downwelling irradiance is low (or in coastal turbid waters). This gave
us an unexpected opportunity to test if complex patterns only occur at
relaxed predation risk since below 200 m the log radiance of downwelling
light can be expected to decrease linearly with depth, which allows
visual modelling to be performed28.
We
showed that PAP is negatively correlated with body size, which
according to our findings suggests that the size of bioluminescent
sharks increases with depth. This observed trend agrees with previous
studies that showed a depth-related increase in size for scavenging bony
fishes39 and small-sized (< 1 m TL) sharks40.
In the water column where food availability decreases with depth, a
larger size is believed to represent a metabolic advantage to scavenge
in the deep sea's oligotrophic environment39.
However, our dataset contains only similarly aged specimens i.e.
specimens close to maturity. Future work will be needed to determine if
the PAP−interpectoral distance relationship is conserved across other
size classes (e.g. neonates) since intraspecific variations in PAP may
occur, notably in response to growth-related morphological changes12, 41.
The results of our predation risk modelling (Fig. 4c)
closely agree with our predictions; bioluminescent sharks do not
display complex patterns when highly exposed to predation. Furthermore, T. kabeyai and S. laticaudus, for which mass captures (> 5 individuals found in the stomach of a single predator) were reported23, 42
occupy the high-risk area of the plot, which confirms the validity of
our approach. Our model also sets a lower PAP limit for lateral markings
to occur, which supports the idea that signalling photophores evolved
by co-option of the initial counterilluminating camouflage. Indeed, at
very low PAP, the lateral photophore coverage is too low to form the
cohesive lateral markings required for signalling, due to the
counterillumination-optimized centripetal density gradient.
Interestingly, in our morphological plot (Fig. 4c),
species with complex photophore patterns separate from all the others.
This trend indicates a strong evolutionary pressure to turn the
counterilluminating pattern into a signalling mechanism when predation
pressure is low and emphasizes the importance of bioluminescent
communication for sharks in the permanent darkness of the deep sea.
The cookiecutter shark I. brasiliensis fits in the middle of the minimum convex polygon of species with lateral markings (Fig. 4c).
This species occupies a peculiar position among sharks and Dalatiidae
since it employs an unusual feeding mode (kleptoparasitism) and displays
a pigmented photophore-free area around the neck2, 10.
Ventrally, this “dog collar” disrupts the counterilluminating pattern
and has been hypothesized to act as a lure by mimicking the search image
of some pelagic predators on which the shark feeds10.
However, no experimental or behavioural data exist to support this
hypothesis and numerous common preys of the shark are either
filter-feeders43, 44 or megacarnivorous organisms44, 45 for which such a mechanism is useless. We propose here an alternative explanation; the dark collar of I. brasiliensis might actually serve as a method of intraspecific recognition functionally analogous to the etmopterid lateral markings.
From
an evolutionary point of view, shark photophores appear to be
exceptional structures. They are part of an unusual isolume-constrained
counterillumination system that constitutes a powerful speciation
driver. Indeed, subtle changes in PAP are associated with important
iso-luminance depth shifts, which can eventually lead to allopatric
speciation. In addition, shark photophores also provide the basis of an
intraspecific bioluminescent recognition tool that favours sympatric (or
parapatric) speciation under relaxed predation risk. We assume these
two complementary mechanisms to have powered the rapid radiation of
bioluminescent sharks in the deep-sea13.
Photophore variables and daytime capture depthVentral skin patches (~0.25 cm2) were excised from the centre of the maximum ventral photophore density area of specimens from 37 distinct species (Supplementary Data 1)
and photographed under a binocular microscope (Leica MZ6, Wetzlar,
Germany). Pictures were analysed in Image J v. 1.46 with random 2 × 2 mm
counting frames (except for T. kabeyai where a 1 × 2 mm counting frame was used instead) to estimate photophore mean diameter, photophore density and PAP (Supplementary Fig. S1); photophore variables were independently measured twice and results were averaged to provide final values.
The
relationship between these photophore variables and capture depth was
investigated in some specimens, selected according to several criteria:
(i) daytime capture i.e. solar elevation ≥ 0° (so that little variation
in downwelling solar irradiance can be assumed47);
(ii) capture depth range (i.e. the difference between the minimum and
maximum depth of a fishing event) ≤ 76 and ≤ 50 m in clear oceanic and
turbid coastal waters, respectively (to restrict the uncertainty on the
residual solar irradiance intensity at capture depth to a single order
of magnitude28, 34)
and (iii) specimen is mature or maturing i.e. neonates are excluded.
When different specimens of a species were available for analysis, the
specimen with the smallest capture depth range was selected (we assumed
that trawled specimens were not captured during the trawling
descent/ascent phase); the capture depth was defined as the median depth
of the capture depth range. Solar elevation at capture locations was
determined from NASA's solar calculator. Water type at capture locations
was determined using SeaWIFS chlorophyll maps: we considered waters
with near-surface [chlorophyll a] inferior to 0.3 mg m−3 to
be ‘oceanic’ while others were classified as ‘coastal’. Turbid coastal
waters absorb residual light quicker than clear oceanic waters, which
means that a same residual solar light level is found at shallower depth
in coastal waters. To compare all the specimens on a standard basis, we
therefore replaced coastal capture depth values by their theoretical
equivalent oceanic capture depth values (for a given residual solar
light level) using downwelling radiance attenuation values from Nilsson
et al.27 i.e. 1.638 and 2.29 log units per 100 m for oceanic and coastal waters, respectively27.
Photophore variables were log-transformed and linearly regressed
against log-transformed oceanic capture depth. Since we cannot exclude
the possibility that some shark photophores may not be functional, which
could induce biases in the analyses, we also conducted the same
analyses considering only confirmed luminous species2, 6, 7, 29, 35, 48, 49, 50.
In addition, we also calculated a theoretical relationship for
hypothetical sharks with photophores that would be iso-luminant across
species (i.e. photophores that would produce the same light intensity
for a given surface area), considering, to facilitate visual comparison
with empirical data, shark photophore luminance to be equal to T. kabeyai photophore luminance at its occurrence depth (284 m), which was determined from the PAP−capture depth relationship (cfr. Fig. 3c). To calculate T. kabeyai photophore luminance, we simply divided downwelling light intensity at 284 m (2.649 × 1014 quanta m−2 s−1 sr−1, cfr. Supplemental Information from Nilsson et al.28) by T. kabeyai. PAP (~56%), which gave us a shark photophore luminance value per PAP unit (4.73 × 1012 quanta m−2 s−1 sr−1 %−1).
The PAP of each other shark was finally multiplied by this luminance
value and compared with depth-related downwelling light intensity (cfr. Supplemental Information from Nilsson et al.28) to determine theoretical occurrence depth of other sharks.
Predation risk modellingTo quantify the adaptive advantage of counterillumination in sharks, we used a recent theory for vision in pelagic habitats28
to calculate the maximum detection distance at which a predator could
see (upward-looking direction) etmopterid and dalatiid sharks if these
sharks did not have counterilluminating photophores (hence appeared as
black targets). According to this theory, three main parameters are
required to calculate observer detection distance (see equation 7 in Supplemental Information from ref. 28):
target diameter, observer pupil diameter and observer depth. Target
diameter was assumed to correspond to interpectoral distance since from
below, this distance provides a feeding-state independent proxy for the
maximum width of a circular pixel fitting into the silhouette of a
bioluminescent shark (Supplementary Fig. S3). Observer pupil diameter was set to 30 mm, the maximum value reported for the swordfish (Xiphias gladius)51
that we chose as a reference predator since (i) large piscivorous
fishes have been reported to prey massively on some bioluminescent
sharks23, 42 and (ii) this fish, which forages into the mesopelagic zone52, also displays the upper bound value for fish pupil diameter28
hence, according to our model, provides a maximum theoretical detection
distance value for a predatory fish. Photoreceptor cell diameter, which
plays a negligible role in the modelling, was set to 3 μm. We
calculated observer depth from target depth, which corresponds to
observer depth − detection distance. We finally performed a log-log plot
of PAP (proxy for target depth, see PAP−capture depth relationship from
Fig. 3c)
against interpectoral distance (proxy for target pixel diameter) for
specimens of 37 distinct species with superimposed isometric detection
distance lines. We expressed detection distance in relative value i.e.
as a multiple of interpectoral distance to account for prey size, which
directly impacts prey escape speed and hence predation risk.
Statistics
Slope
comparisons were performed using ANCOVAs. All statistical analyses were
performed in JMP® v. 10 and considered to be significant at the 0.05
level. Mean value of photophore diameter, photophore density and PAP are
indicated ±SEM.
Claes, J. M. & Mallefet, J. in Bioluminescence in Focus – a Collection of Illuminating Essays (ed. Meyer-Rochow, V. B.) 51–65 (Research Signpost, Kerala, 2009).
Claes, J. M., Sato, K. & Mallefet, J.Morphology and control of photogenic structures in a rare dwarf pelagic shark (Etmopterus splendidus). J. Exp. Mar. Biol. Ecol.406, 1–5 (2011).
Hubbs, C. L., Iwai, T. & Matsubara, K.External and internal characters, horizontal and vertical distribution, luminescence, and food of the dwarf pelagic shark, Euprotomicrus bispinatus. Bull. Scripps Inst. Oceanogr.10, 1–64 (1967).
Last, P. R., Burgess, G. H. & Séret, B.Description of six new species of lantern-sharks of the genus Etmopterus (Squaloidea: Etmopteridae) from the Australasian region. Cybium26, 203–223 (2002).
Straube, N., Iglésias, S. P., Sellos, D. Y., Kriwet, J. & Schliewen, U. K.Molecular phylogeny and node time estimation of bioluminescent lantern sharks (Elasmobranchii: Etmopteridae). Mol. Phylogenet. Evol.56, 905–917 (2010).
Johnsen, S., Widder, E. A. & Mobley, C. D.Propagation and perception of bioluminescence: factors affecting counterillumination as a cryptic strategy. Biol. Bull.207, 1–16 (2004).
Denton, E. J., Herring, P. J., Widder, E. A., Latz, M. F. & Case, J. F.The role of filters in the photophore of oceanic animals and their relation to vision in the oceanic environment. Proc. Roy. Soc. B225, 63–97 (1985).
Claes, J. M. & Mallefet, J.Early development of bioluminescence suggests camouflage by counter-illumination in the velvet belly lantern shark Etmopterus spinax (Squaloidea: Etmopteridae). J. Fish Biol.73, 1337–1350 (2008).
Claes, J. M., Aksnes, D. L. & Mallefet, J.Phantom hunter of the fjords: counterillumination in a shark (Etmopterus spinax). J. Exp. Mar. Biol. Ecol.388, 28–32 (2010).
Claes, J. M., Dean, M. N., Nilsson, D.-E., Hart, N. S. & Mallefet, J.A deepwater fish with ‘lightsabers’ – dorsal spine-associated luminescence in a counterilluminating lanternshark. Sci. Rep.3, 1308 (2013).
Claes, J. M. & Mallefet, J.Functional physiology of lantern shark (Etmopterus spinax) luminescent pattern: differential hormonal regulation of luminous zones. J. Exp. Biol.213, 1852–1858 (2010).
Klug, S. & Kriwet, J.Timing of deep-sea adaptation in dogfish sharks: insights from a supertree of extinct and extant taxa. Zool. Scr.39, 331–342 (2010).
Naylor, G. J., Caira, J. N., Jensen, K., Rosana, K. A., Straube, N. & Lakner, C. in The Biology of Sharks and Their Relatives (eds. Carrier, J. C., Musak, J. A. & Heithaus, M. R.) 31–56 (2012).
Yano, K., Mochizuki, K., Tsukada, O. & Suzuki, K.Further description and notes of natural history of the viper dogfish, Trigonognathus kabeyai from the Kumano-nada Sea and the Ogasawara Islands, Japan (Chondrichthyes: Etmopteridae). Ichthyol. Res.50, 251–258 (2003).
Young, R. E., Kampa, E. M., Maynard, S. D., Mencher, F. M. & Roper, C. F.Counterillumination and the upper depth limits of midwater animals. Deep Sea Res.27, 671–691 (1980).
Jones, B. W. & Nishiguchi, M. K.Counterillumination in the Hawaiian bobtail squid, Euprymna scolopes Berry (Mollusca: Cephalopoda). Mar. Biol.144, 1151–1155 (2004).
Claes, J. M.Function and control of luminescence from lanternshark (Etmopterus spinax) photophores. Ph. D. Thesis. Université catholique de Louvain (Belgium, 2010).
Johnsen, S., Frank, T. M., Haddock, S. H., Widder, E. A. & Messing, C. G.Light and vision in the deep-sea benthos: I. Bioluminescence at 500–1000 m depth in the Bahamian Islands. J. Exp. Biol.215, 3335–3343 (2012).
Claes, J. M., Krönström, J., Holmgren, S. & Mallefet, J.Nitric oxide in the control of luminescence from lantern shark (Etmopterus spinax) photophores. J. Exp. Biol.213, 3005–3011 (2010).
Collins, M. A., Bailey, D. M., Ruxton, G. D. & Priede, I. G.Trends
in body size across an environmental gradient: a differential response
in scavenging and non-scavenging demersal deep-sea fish. Proc. Roy. Soc. B272, 2051–205 (2005).
Sadowsky, V., Amorim, A. D. & Arfelli, C. A.Record of unusual number of dwarf shark, Squaliolus laticaudus, off the south coast of Brazil. Bol. Inst. Pesca12, 45–50 (1985).
Berra, T. M. & Hutchins, J. B.A specimen of megamouth shark, Megachasma pelagios (Megachasmidae) from Western Australia. Rec. West. Aust. Mus.14, 651–656 (1990).
Dwyer, S. L. & Visser, I. N.Cookie cutter shark (Isistius sp.) bites on cetaceans, with particular reference to killer whales (orca)(Orcinus orca). Aquat. Mamm.37, 111–138 (2011).
Hoyos-Padilla, M., Papastamatiou, Y. P., O'Sullivan, J. & Lowe, C. G.Observation of an attack by a cookiecutter shark (Isistius brasiliensis) on a white shark (Carcharodon carcharias). Pac. Sci.67, 129–134 (2013).
West, M. J., Slomianka, L. & Gundersen, H. J. G.Unbiased
stereological estimation of the total number of neurons in the
subdivisions of the rat hippocampus using the optical fractionator. Anat. Rec.231,182–497 (1991).
Takahashi, M., Okamura, H., Yokawa, K. & Okazaki, M.Swimming behavior and migration of a swordfish recorded by an archival tag. Mar. Freshwater Res.54, 527–534 (2003).
We thank H.-C. Ho and K. Sato as well as the staffs of
National Museum of Marine Biology and Aquarium and Okinawa Churaumi
Aquarium for help in live specimen collection and maintenance. Access to
preserved collection specimens and their capture information would not
have been possible without the help of G. Burgess, R. Causse, G.
Duhamel, A. Graham, H.-C. Ho, T. Kawai, S. Morrison, R. Robins, K. Sato,
U. Schliewen, B. Séret, R. Singer, M. Stehmann, R. Thiel, S. Weigmann
and H. Zidowitz. We also acknowledge E. Garza Gisholt for his help in
using his R script for the creation of photophore maps. Financial
support (including grant: 1.5.278.08) was provided by the Fonds National
de la Recherche Scientifique (FNRS, Belgium) to J.M.C. (postdoctoral
researcher at FNRS) and J.M. (research associate at FNRS). D.-E.N.
acknowledge The Swedish Research Council (grant: 2011-4768) and the Knut
and Alice Wallenberg Foundation (grant: Ultimate Vision). G.J.P. Naylor
and the National Science Foundation are gratefully acknowledged for
support to N.S. (grant: NSF, DEB 1132229). Part of the research was
supported by the Australian Research Council (grant: DP110103294) to
S.P.C. This is a contribution to the Biodiversity Research Center (BDIV)
and to the Centre Interuniversitaire de Biologie Marine (CIBIM).
Laboratoire de Biologie Marine, Earth and Life Institute, Université catholique de Louvain, 1348 Louvain-la-Neuve, Belgium
Julien M. Claes &
Jérôme Mallefet
Lund Vision Group, Lund University, 22362 Lund, Sweden
Dan-Eric Nilsson
Department of Biology, College of Charleston, Charleston, SC 29412, USA
Nicolas Straube
The School of Animal Biology and The Oceans Institute, The University of Western Australia, Crawley, WA 6009, Australia
Shaun P. Collin
Contributions
J.M.C. and J.M. collected live sharks, took photographs and measured in vivo
luminescence physical characteristics. J.M.C. performed the
morphological measurements of preserved specimens with the assistance of
N.S. and S.P.C. D.E.N. and J.M.C. established the predation risk
modelling. J.M.C. performed the analyses and wrote the manuscript. All
authors discussed the results and commented on the manuscript at all
stages.
Competing financial interests
The authors declare no competing financial interests.
