Comparisons of SSD in marine with non-marine aquatic turtles
Regression Approach .- Figure 2 illustrates separate regressions
of male versus female body size for marine and NMAT with 95% confidence
intervals and the 1:1 line (null hypothesis) for comparison. The
regression for marine turtles using only the species-mean data (Fig. 2A)
was: male CL = -2.4647 + 1.0014 (female CL) adj
r2=0.99, p<0.0001). Neither the slope nor
the intercept differed significantly from the null expectation (slope:
t(4)=-0.001, tcrit=2.267, p=0.99; intercept:
t(4)=-1.874, tcrit=2.267, p=1). The 95% confidence
intervals of this regression overlap or encompasses the 1:1 line.
By contrast, NMAT exhibit a wide range of departures from equality in
size, mostly in the direction of larger female size (Fig. 2A), which is
reflected by a slope of 0.76. The 95% confidence intervals overlap the
1:1 line only in the domain of the very smallest species
(<~15cm CL). The ANOVA (Table 1a) indicated an
overall significant effect of female size on male size, but also a
significant interaction between female size and habitat, indicating that
this effect differed between marine and non-marine habitats. In other
words, in conjunction with the results of the regressions, this means
that females are on average larger than males in NMAT, but sexes do not
differ in size in marine turtles.
SDILGF Approach .- Figure 2B illustrates
SDILGF values for all 94 species of aquatic turtles (87
non-marine, seven marine). The values for marine turtles are very close
to or overlapping the null expectation of no sexual size dimorphism
(SDILGF = 0). The mean SDILGF for marine
turtles was 0.027 ± 0.0103, and ranged from 0.002 to 0.067, whereas the
mean SDILGF for NMAT was an order of magnitude higher
and biased towards females (0.337 ± 0.0419, range -0.215 to 1.684).
ANOVA (Table 1b) indicated that these distributions were significantly
different (F1,92=4.339, p=0.04). Furthermore, the range
of values was considerably larger in non-marine turtles (1.899) than in
marine species (0.066).
DISCUSSION
Our comprehensive review of the literature permitted the first
definitive statistical evaluation of the degree of SSD in marine
turtles, reflecting information from all seven extant species. Our
analysis revealed a striking lack of SSD (Fig. 1), a pattern that is
notably distinct from NMAT, which typically exhibit female-biased SSD
(Fig. 2). Female-biased SSD is typically interpreted as a response to
fecundity selection, in the absence of male combat, which should result
in larger male size via sexual selection (Berry & Shine, 1980). Marine
turtles do not exhibit male combat and therefore would be expected to
exhibit female-biased SSD, with all other conditions remaining the
same. Whatever the sources of selection, differences between
sexes in body size arise due to differences in growth rates over the
same prematuration interval or due to differences in the prematuration
duration of growth (Bernardo, 1993; Cox & John-Alder, 2007; J. Stamps
& Krishnan, 1997; J. A. Stamps, 2008). A third possibility is
differential, size-specific mortality that influences one sex more than
the other(DeGregorio, Grosse, & Gibbons, 2012; Roosenburg, 1991). The
lack of SSD in marine turtles thus requires an understanding of what
kind of selection is prohibiting differentiation in size between sexes.
We suggest that this is due to both the high energetic cost of
locomotion in the marine environment coupled with frequent long-distance
movements by both sexes.
It is well-established that the marine environment imposes strong
selection on body form of large, widely-foraging vertebrates (Frank E
Fish, 1993, 1998; Frank E. Fish, Howle, & Murray, 2008; Kelley &
Pyenson, 2015; Seibel & Drazen, 2007; Webb, 1988; Webb & De Buffrénil,
1990; Williams Terrie, 1999), driven principally by selection for drag
reduction and therefore cost-efficient swimming (Frank E Fish, 1993,
1998; Webb, 1988; Williams Terrie, 1999). Saltwater is denser and has
both higher dynamic and kinematic viscosities than freshwater (Vogel,
1994). Consequently, we would expect from first principles that the
marine environment establishes a different selective milieu on sexual
dimorphism.
Marine turtles are morphologically distinctive among all aquatic turtles
in several ways. First, marine turtle limbs reflect strong selection for
specialised locomotion, both in form and in function. While all limbs
are modified into flippers, the forelimbs are hypertrophied and modified
into broad, distally tapered, rigid, wing-like flippers (Davenport,
Munks, & Oxford, 1984; Renous, de Broin, Depecker, Davenport, & Bels,
2007; Wyneken, 1997). Apart from the external wing-like shape itself,
the underlying bony architecture is distinct in marine turtles (Renous
et al., 2007). In particular, the humerus is flattened compared to other
turtles (Renous et al., 2007; Wyneken, 1997) and biomechanical analyses
indicate that this confers great strength and hydrodynamic efficiency
(Dickson & Pierce, 2019).The locomotory pattern of marine turtles
consists of a synchronous upward/downward sweeping motion of the fore
flippers that generates thrust (Davenport et al., 1984; Wyneken, 1997),
similar to the pattern in other marine tetrapods that have flippers
(Clark & Bemis, 1979; Walker, 2002). That such derived flippers have
convergently evolved across multiple lineages of other marine tetrapods,
including seals, penguins, and plesiosaurs (Wyneken, 1997), indicates
strong selection for efficient long-distance swimming. It is well
established from mathematical modelling that flapping appendages in
large aquatic animals permit efficient and rapid propulsion (Blake,
1981; Walker, 2002; Walker & Westneat, 2000).
The second morphological specialisation of marine turtles is the
extraordinary streamlining of their body form (Davenport et al., 1984;
Wyneken, 1997). This stereotypic streamlining is evident throughout
their evolutionary history including the oldest known definitive
species, Desmatochelys padillai (Cadena & Parham, 2015), and
across an order of magnitude range in body size from the smallest living
species Lepidochelys kempii (~63 cm
carapace length) to the largest known species, the extinctArchelon ischyros (Wieland, 1896), which exceeded 400 cm in
carapace length. A further adaptation evident in D. coriacea are
the longitudinal dorsal ridges on the carapace that enhance hydrodynamic
performance (Bang, Kim, Lee, & Choi, 2016).
Taken together, these specialisations indicate that selection has
optimised marine turtle morphology for energetically efficient swimming.
Indeed, a key feature of marine turtle biology is their capacity to
exploit resources across vast geographic expanses. Both sexes of all
seven species of marine turtles undertake long-distance, sometimes
trans-oceanic migrations covering many hundreds to thousands of
kilometers (Boyle et al., 2009; Graeme C Hays, Houghton, & Myers, 2004;
Graeme C. Hays, Mortimer, Ierodiaconou, & Esteban, 2014; Graeme C. Hays
& Scott, 2013; Luschi, Hays, & Papi, 2003; Plotkin, 2003, 2010;
Shillinger et al., 2008). Two species (D. coriacea and L.
olivacea ) are oceanic, pelagic, widely-foraging predators (Graeme C
Hays et al., 2004; Plotkin, 2010; Shillinger et al., 2008). Satellite
tagging studies show that D. coriacea achieves a mean speed of
33-49 km/d, with a maximum of 62 km/d (Shillinger et al., 2008) andL. olivacea a mean of 28.32 km/d and a maximum of 79.4 km/d
(Plotkin, 2010).
Despite their having evolved unique morphology among turtles for
efficient swimming, this high vagility lifestyle still entails
substantial energetic expenditure. Unfortunately, few quantitative data
on the energetic requirements of swimming in adult marine turtles are
available. However, Prange (1976) studied the metabolic cost of swimming
in juvenile Chelonia mydas . By extrapolating these costs, he
estimated that the energetic demand for a long-distance migration of
adults between breeding and feeding grounds would require approximately
21% of their body mass in fat stores. Given the common body form and
long-distance movement of all marine turtle species, it is not
far-fetched that these energy requirements are incurred by all of the
species.
Because the high energetic costs of sustained swimming are incurred by
both sexes, neither sex can allocate significant energy to continued
growth after maturation and therefore neither sex can achieve a larger
size than the other (Bernardo, 1993; Cox & John-Alder, 2007; J. Stamps
& Krishnan, 1997; J. A. Stamps, 2008). For instance, female-biased SSD
is usually attributed to fecundity selection, but the ability for female
marine turtles to allocate energy to enhanced post-maturation growth in
response to fecundity selection appears to be prohibited by their costly
locomotion. An analysis of growth rates in different populations of
loggerhead turtles instantiates that the cost of achieving larger size
comes at the expense of reproductive frequency (Hatase & Tsukamoto,
2008). Thus, the capacity to continue to grow and produce eggs come into
close conflict because of the energetic background costs of locomotion
(Hatase & Tsukamoto, 2008). A further indication that marine turtles
lack discretionary energy for continued growth that could produce SSD is
found in their unusual post-maturation growth patterns. Marine turtles
exhibit determinate-like growth (Omeyer, Fuller, Godley, Snape, &
Broderick, 2018), a pattern which is unlike other turtles (Congdon,
Gibbons, Brooks, Rollinson, & Tsaliagos, 2013; Gibbons, Semlitsch,
Greene, & Schubauer, 1981; Lindeman, 1999) and in fact unlike most
other ectotherms (Bernardo, 1993; Gotthard, 2001; Sebens, 1987; Tilley,
1980) which exhibit indeterminate growth.
In conclusion, our study demonstrated that, unlike NMAT, marine turtles
are not sexually size dimorphic, and we argued that this difference is
due to the distinct selective milieu imposed by the oceanic environment.
Hence, future studies should acknowledge this distinction and no longer
group marine turtles with NMAT as numerous studies have previously done.
We also note that, where data are available for multiple populations of
the same species (Figure 1A), the magnitude and direction of SSD vary.
This indicates that the common practise of basing a species-level trait
estimate on a single population likely introduces error variance in
comparative datasets. Further, we note that in our comprehensive
dataset, the sample size for females was more than 20 times that for
males, and in the case of N. depressus , only a single male has
been measured. This unbalanced sample size between sexes is likely due
to the oversampling of nesting fmales; future studies need to be
deliberate about acquiring male data on marine turtle males.
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Table 1. Analyses of Variance
(ANOVAs) modelling the degree of difference in body size between males
and females in non-marine versus marine turtles. (a) Analysis of mean
body size between males and females (b) Analysis of
SDILGFvalues.