Elephants develop wrinkles through both form and function

Abstract

The trunks of elephants have prominent wrinkles from their base to the very tip. But neither the obvious differences in wrinkles between elephant species nor their development have been studied before. In this work, we characterize the lifelong development of trunk wrinkles in Asian and African elephants. Asian elephants have more dorsal major, meaning deep and wide, trunk wrinkles (approx. 126 ± 25 s.d.) than African elephants (approx. 83 ± 13 s.d.). Both species have more dorsal than ventral major trunk wrinkles and a closer wrinkle spacing distally than proximally. In Asian elephants, wrinkle density is high in the 'trunk wrapping zone'. Wrinkle numbers on the left and right sides of the distal trunk differed as a function of trunk lateralization, with frequent bending in one direction causing wrinkle formation. Micro-computed tomography (microCT) imaging and microscopy of newborn elephants' trunks revealed a constant thickness of the putative epidermis, whereas the putative dermis shrinks in the wrinkle troughs. During fetal development, wrinkle numbers double every 20 days in an early exponential phase. Later wrinkles are added slowly, but at a faster rate in Asian than African elephants. We discuss the relationship of species differences in trunk wrinkle distribution and number with behavioural, environmental and biomechanical factors.

Keywords: Proboscidea; ageing; development; morphology; ontogeny.

Figure 1.

Asian (E. maximus) and African (L. africana) elephants differ in trunk morphology, including trunk wrinkles. (a) Drawing of the trunk of an adult Asian elephant. Note the larger number of transversal wrinkles in the Asian elephant compared with the African elephant trunk in (h). (b) Proximal trunk base wrinkles of an Asian elephant. (c) Same as (b) but for the middle part of the trunk. (d) Same as (b) but for the distal part of the trunk. (e–g) Same as (b–d) but for an African elephant. (h) Drawing of the trunk of an adult African elephant. Note the major wrinkles on the proximal half of the trunk that fold over each other and how they transition to the tightly packed distal trunk wrinkles. Illustrations (a,h): Cindy Ritter. Photo credit (b–d): Lena Kaufmann, Humboldt Universität zu Berlin; Zoologischer Garten Berlin, Berlin, Germany. Photo credit (e–g): Lena Kaufmann, Humboldt Universität zu Berlin; Zoo Schönbrunn, Vienna, Austria.

Figure 2.

Transversal trunk major and minor wrinkles differ in counts and distribution between Asian and African elephants. (a) Female Asian elephant Carla (Zoo Berlin) next to a tracing of minor and major wrinkles with a schematic of what minor/major wrinkles look like in Asian elephants. Major wrinkles in contrast to minor wrinkles are deeper, more regularly occurring, and regularly spaced, and transverse the whole dorsal or ventral trunk. Note the zero-line between the eyes, wrinkles proximal to this were not included in the analysis. (b) Same as (a) but for female African elephant Drumbo (at the time of photograph Zoo Schönbrunn). (c) Comparison of trunk wrinkle numbers between Asian and African elephants in babies (left) and adults (right). Asian elephant babies (n = 3) and African elephant babies (n = 2) have similar numbers of minor and major wrinkles. Asian adult elephants (n = 7) have more major trunk wrinkles (x̄ = 126, s.d. = 25) than African adult elephants (n = 7, x̄ = 83, s.d. = 13; two-sample t‐test t(12) = 4.05, d = 2.16, p = 0.003). Circle = female, triangle = male, diamond = unknown. (d) Positions of minor (left) and major (right) wrinkles on trunks normalized to total trunk length in individual female Asian (n = 3) and African (n = 5) elephants. (e) Heatmaps showing the distribution of minor (left) and major (right) trunk wrinkles in Asian (n = 3) and African (n = 5) elephants, based on (d). Heatmaps show average density of wrinkles, wrinkle positions are normalized to trunk length. Asian elephants have on average more minor wrinkles in the proximal part of the trunk, whereas in African elephants minor wrinkles are more spread over the rest of the trunk. Asian elephants have on average more major wrinkles in the distal half of the trunk with a particularly high density in the region where they bend when wrapping objects. Blue shows a low average density of wrinkles and red a high average density of wrinkles at this position of the trunk. (f) On the left, a photograph of an African elephant baby trunk showing tracings of major wrinkles on the dorsal (upper) and ventral (lower) sides of the trunk. On the right, a comparison of major wrinkles on the dorsal and ventral sides of the same trunk in Asian (n = 3) and African (n = 2) elephants. There are significantly more wrinkles on the dorsal (x̄ = 77, s.d. = 10) than on the ventral sides of the trunks (x̄ = 47, s.d. = 7; two-tails paired t‐test t(4) = 5.07, d = 2.27, p = 0.007). Circle = female, triangle = male, diamond = unknown. The line between symbols represents both symbols being part of the same trunk, one being the winkle number on the dorsal and one the wrinkle number on the ventral side. Photo credit (a): Lena Kaufmann, Humboldt Universität zu Berlin; Zoologischer Garten Berlin, Berlin, Germany. Photo credit (b): Lena Kaufmann, Humboldt Universität zu Berlin; Zoo Schönbrunn, Vienna, Austria. Photo credit (f): Lena Kaufmann, Humboldt Universität zu Berlin.

Figure 3.

Left- and right-trunkers have more wrinkles on the left and right trunk sides, respectively (a) Image of a left-trunker with the trunk tip and distal trunk shaft of an Asian elephant. Note the shorter whiskers on the right side and the longer whiskers on the left side of the distal trunk shaft. Modified from Deiringer et al. [49]. (b) Image showing a left-trunker behaviour of an Asian elephant reaching for a watermelon. The image displays a trunk wrapping to the left with the right-side of the distal shaft of the trunk in contact with the ground which results in whisker abrasion. Modified from Deiringer et al. [49]. (c) African elephant trunk tip and distal trunk shaft, in red the major wrinkles on the trunk shaft that were counted. The red line crossing the tip is the last wrinkle counted. (d) Univariate plot of the fraction of wrinkles (normalized to the total count on both trunk sides) on the trunk side with shorter or longer whiskers. Trunk function is lateralized in elephants and so-called left-trunkers, who preferentially grasp towards the left side, have shorter whiskers of the right side of the distal trunk shaft [49]; the reverse is true for right-trunkers. We observed approximately 10% more wrinkles on the longer whisker side. In yellow, the wrinkles fraction on the longer whisker side and in blue, the wrinkles on the shorter whisker side. One dot is one animal, yellow and blue for the same animal plotted on the same axis. Wrinkle counts are reported as percentage of total wrinkles on the respective trunk shaft specimen. Paired sample t‐test t(14) = 2.59, d = 0.67, p = 0.022. n = 5 adult African elephants, 9 adult Asian elephants. (e) Univariate plot of the fraction of wrinkles (normalized to the total count on both trunk sides) on the left or right side of the trunk. The full dots are the wrinkles fraction on the left side and the empty dots are the wrinkles on the right side. One dot is one animal, for the same animal the dots are plotted on the same axis. n = 5 adult African elephants, 9 adult Asian elephants. Photo credit (a,b,c): Lena Kaufmann, Humboldt Universität zu Berlin.

Figure 4.

Visualization of trunk wrinkles in microCT scans of an Asian and an African baby elephant trunk. (a) Volume rendering of a microCT-scanned Asian baby elephant trunk. (b) Sagittal slice of an Asian baby elephant trunk. (c) High magnification view of proximal dorsal wrinkles in the Asian baby elephant trunk. Note the constant thickness of the putative epidermis, while the putative dermis is getting thinner in the troughs of the wrinkles. The two primary load-bearing layers of skin are highlighted; the epidermis in blue, and the dermis in pink. (d) High magnification view of distal dorsal wrinkles in the Asian baby elephant trunk with highlights of the two primary load-bearing skin layers. Note the constant thickness of the putative epidermis, while the putative dermis is getting thinner in the troughs of the wrinkles. (e) Volume rendering of a microCT-scanned African baby elephant trunk. (f) Sagittal slice of an African baby elephant trunk. (g) High magnification view of dorsal wrinkles in the African baby elephant trunk. Note the constant thickness of the putative epidermis, while the putative dermis is getting thinner in the troughs of the wrinkles. The two primary load-bearing layers of skin are highlighted similarly to (c) and (d).

Figure 5.

Wrinkle amplitude and wavelength of African and Asian elephant baby trunks. (a) Wavelength of an Asian baby elephant (blue) trunk and an African baby elephant (maroon) trunk, taken from the microCT-scans in figure 4. Averages of three different proximal, mid-section and distal sections are shown with shaded sections where the average of the wrinkle amplitude and wavelength are compared statistically in each section. Statistics for the three sections are shown on the right. The African baby elephant has significantly larger wavelengths in the mid-section (x̄ = 5.98 mm, s.d. = 1.43 mm; one-way ANOVA F = 32.93, p < 0.001) and distal section (x̄ = 3.29 mm, s.d. = 0.88 mm; one-way ANOVA F = 6.98, p = 0.01) compared with the Asian baby elephant’s mid-section (x̄ = 3.64 mm, s.d. = 0.86 mm) and distal section (x̄ = 2.68 mm, s.d. = 0.56 mm). (b) Crest-to-crest amplitude of an Asian baby elephant (blue) trunk and an African baby elephant (maroon) trunk, taken from the microCT scans in figure 4. The average of different zones is shown similarly to (a) with comparisons between the species. Statistics for the three sections are shown on the right. The Asian baby elephant has significantly higher amplitudes along the whole trunk including proximal (x̄ = 2.71 mm, s.d. = 0.42 mm; one-way ANOVA F = 22.5, p < 0.001), mid-section (x̄ = 1.86 mm, s.d. = 0.35 mm; one-way ANOVA F = 44.68, p < 0.001), and distal (x̄ = 1.45 mm, s.d. = 0.48 mm; one-way ANOVA F = 11.87, p = 0.001) sections. This is compared with the African baby elephant with amplitudes decreasing by nearly 35% along the trunk from the proximal section (x̄ = 1.62 mm, s.d. = 0.32 mm), to the mid-section (x̄ = 1.12 mm, s.d. = 0.22 mm) and to the distal portion (x̄ = 1.05 mm, s.d. = 0.22 mm).

Figure 6.

Fetal trunk and trunk wrinkle development. (a) Schematic drawings of African elephant fetuses. Grey, outline of the head and wrinkles; grey dashed, putative wrinkles; black, outline of the trunk; green, lower lip; red, upper lip. Fetuses were redrawn from references following references [–48]. E# indicates the embryonic age of the photo with the number indicating days. (b) Schematic of stages of fetal wrinkle development in African and Asian elephants. (c) Schematic of stages of fetal lip development in African elephants. (d) Relative length growth of various body parts in African elephants. Length was normalized to the length of the respective body part in E80 fetuses and is given in per cent. The trunk grows more than other body parts and the accelerated growth occurs mainly between E60 and E150. (e) Trunk length growth in African and Asian elephants is similar. (f) Wrinkle development in African and Asian elephants. Wrinkle number increases in sharply different phases: Between E80 and E130, there is an exponential increase in wrinkle number with a doubling time of approximately 20 days. After E130 addition of wrinkles is slow, but slightly faster in Asian than in African elephants. Note that wrinkles could only be counted in a subset of fetuses.

Figure 7.

Fetal trunk finger development in Asian and African elephants. (a) Schematic of stages of trunk tip development in African and Asian elephants. (b) Length difference of dorsal and ventral trunk finger in African elephants throughout fetal development. Pre-E120, there are no fingers, then the ventral finger is longer (highlighted as red dots) and after E200, the dorsal finger takes over. (c) Fetal dorsal and ventral finger growth in African elephants. Finger growth goes through a brief exponential phase (E130–E180), after which finger growth slows down. The length of both the dorsal and ventral fingers could not be determined in all specimens. Note that the ventral finger (circles) tends to be longer than the dorsal finger (triangles) in early fetuses and shorter than the dorsal finger in older fetuses.