Cuticle and Eggshell
We found that the Apterygian cuticle consisted of a very thin, waxy,
water repellent mineral layer composed of triangular particles; that at
times, formed aggregations that occluded eggshell pores. We also found
that all the studied species of Apteryx presented plugged or
capped pores. From our observations it seems possible that the cuticle
of Apteryx erodes over time, from a more sealed egg when freshly
laid to a more porous one, as the embryo develops and requires a greater
gas exchange. We also found that many pores did not go all the way
through the eggshell, a similar observation was mentioned by
Silyn-Roberts (1983) nevertheless, the function of these types of pores
is still not clear. Similar pores that do not transverse the eggshells
have been observed in the eggs of Ostriches (Struthio camelus ), a
relative of Apteryx (Willoughby et al., 2016; Maina, 2017).
The cuticle and eggshell mediate the interaction between the developing
embryo and the environment. As such, they are the first barriers against
pathogens and allow gas exchange and water vapour conductance (D’Alba et
al. 2017). Features of the cuticle such as plugs, and caps have been
associated with nesting in humid environments (D’Alba et al. 2016) as
they block the pores. Board (1981) suggested that plugs could also serve
as a physical barrier to defend the egg contents particularly against
waterborne microbes. Apteryx species breed during the austral
winter, which in New Zealand is characterised by frequent and heavy
precipitation (Leathwick et al. 2002); they lay their eggs in burrows
with a relatively humid environment and their incubation period is long.
We found that pluviosity was significantly associated with eggshell
thickness, pore density and pore radius.
A thicker eggshell means longer pores, reducing the number and area of
the pores could be an adaptation to prevent water to penetrate the egg.
This seems even more plausible considering that other adaptations, such
as plugs, and caps seem to point in the same direction. Apteryxnests are frequently holes in the ground, this, with an incubating
parent that could return to the nest with a wet plumage seems to
indicate that the kiwi incubates in a very wet environment. Which in
turn it would be expected to increase the humidity of the nest, making
very necessary that future studies measure the humidity of nests in
rainy areas such as Okarito or Haast, areas inhabited by Rowi and
Tokoeka respectively, furthermore, Okarito experiences frequent snow (up
to 1m in the past 10 years); studying the nest architecture of Rowi and
Tokoeka would clarify further the nature of the different
characteristics present in the Apterygian eggshell.
Apteryx does not present the accessory layer described in
Megapodidae, Phoenicopteridae, and Podicipedidae (Tullett et al. 1976,
Board et al. 1984, D’Alba et al. 2017) and that has been associated with
decreasing bacterial penetration in high humidity environments. It seems
that Apteryx might achieve a more sealed egg with a
water-repellent smooth cuticle that erodes as gas diffusion needs
increase with the progression of embryo development.
Temperature and barometric pressure play a very important role in gas
diffusion; higher temperatures and lower pressures allow the gases to
diffuse at faster rates. Water vapour conductance and gas exchange can
be modulated by variations in the number, length, shape, and diameter of
pores and by obstructions in the pores. For example, water vapour
conductance and gas exchange can be lowered by having less pores per
area, longer pores, branched pores, and by increasing the number of caps
and plugs or unperforated pores. Therefore, the number and shape of
pores have been found to be related to incubation period (Zimmermann et
al. 2007), altitude where the birds live (Rahn et al., 1977), and the
nest microclimate (Birchard and Kilgore, 1980).
Eggshell thickness and pore radius showed a moderate to low negative
correlation with barometric pressure. At lower barometric pressures
water diffusivity increases therefore eggs are at higher risk of
desiccation, hence a thicker eggshell and smaller pore would reduce the
water vapour conductance accordingly. The opposite is true for higher
barometric pressures; however, in this case the eggshell must also stand
a greater overall pressure on its structure, therefore a thickened
eggshell would be beneficial. In chickens, a move from an altitude of
3800 masl to 1200 masl resulted in an increased eggshell thickness with
decreased pore radius to compensate for the increase in barometric
pressure (Rahn et al. 1982). Similar correlations occurred between
temperature and eggshell thickness and pore radius.
Eggshell thickness is known to be proportional to the body mass of the
laying bird (Tullett 1978, Birchard and Deeming 2009). However,Apteryx species vary in their incubation behaviour. In Brown Kiwi
the male is the sole incubator, while in Roroa and Rowi both male and
female incubate and in Tokoeka, there are helpers at the nest, requiring
further studies relating both the female and the male body sizes to the
egg and the eggshell, it is worth to notice that the egg mass is very
high in relation to body mass, being 23.6 and 14.6% for A.oweniiand A. australis (possibly A.mantelli ) (Dyke and Kaiser
2010). Apteryx eggshells are allometrically thinner than expected
and this is probably to reduce the weight the female must carry (Calder
1979) and to allow chicks to crack the shell when hatching, asApteryx does not possess an egg tooth (Calder 1978). The
trade-off is then that a thinner eggshell is more prone to mechanical
damage and even hairline fractures have been known to impact embryo
health and development (Sylin-Roberts 1980; Stadelman 1995). In our
study, the lightest (on average) of the four species, the Rowi had a
thicker eggshell than the heavier Brown Kiwi; also, the Roroa, the
heaviest of Apteryx had a thinner eggshell than the lighter Haast
Tokoeka.
We suggest that the different incubation strategy of each species could
also influence the evolution of eggshell thickness. In Tokoeka both
males and females incubate, females are larger than the males and this
could have been a selective pressure for a thicker eggshell that evaded
breakage. In contrast, in the lighter Brown Kiwi generally only the
males incubate. Rowi, being the smallest of the three species, presents
an eggshell thickness similar to that of Haast Tokoeka but in contrast
to Brown Kiwi, both male and female have been observed incubating
(Colbourne 2002).