Palaeohistology reveals a slow pace of life for the dwarfed Sicilian elephant

Abstract

The 1-m-tall dwarf elephant Palaeoloxodon falconeri from the Pleistocene of Sicily (Italy) is an extreme example of insular dwarfism and epitomizes the Island Rule. Based on scaling of life-history (LH) traits with body mass, P. falconeri is widely considered to be 'r-selected' by truncation of the growth period, associated with an early onset of reproduction and an abbreviated lifespan. These conjectures are, however, at odds with predictions from LH models for adaptive shifts in body size on islands. To settle the LH strategy of P. falconeri, we used bone, molar, and tusk histology to infer growth rates, age at first reproduction, and longevity. Our results from all approaches are congruent and provide evidence that the insular dwarf elephant grew at very slow rates over an extended period; attained maturity at the age of 15 years; and had a minimum lifespan of 68 years. This surpasses not only the values predicted from body mass but even those of both its giant sister taxon (P. antiquus) and its large mainland cousin (L. africana). The suite of LH traits of P. falconeri is consistent with the LH data hitherto inferred for other dwarfed insular mammals. P. falconeri, thus, not only epitomizes the Island Rule but it can also be viewed as a paradigm of evolutionary change towards a slow LH that accompanies the process of dwarfing in insular mammals.

Figure 1

P. falconeri GR. (a) sample of the aged tibiae: 1,2: neonates (CAT-106; CAT-108); 3: one year (ELEPH1-T); 4: two years (CAT-124); 5: 3,5 years (CAT-128); 6,7,8: 4 years (CAT-132, Cat 133, ELEPH2-T); 9,10: 7 years (CAT 139, Cat 140); 11,12: 9 years (CAT-45, 142); 13: 12 years (ELEPH3-T); 14: 13 years (CAT-46); 15: 14 years (CAT-179); 16: 18 years (T-181);17: 23 years (Roma 6) (Graphic scale 10 cm). (b) Scaling of mean body mass GR from birth to maturity (MBMGR, expressed in grams/day) in respect to adult body mass, in log10, using phylogenetic generalized least square regressions (PGLS), in a large sample (n = 106) of species of ungulates (see Supplementary material 8 for results of PGLS). Blue dots: ungulates; red dots: P. falconeri (body mass from tibia LTC; Supplementary material 2; Supplementary Tables 2, 3), black dot: Elephas maximus; orange square: L. africana; data from PanTheria. (c) distribution of residuals of the PGLS log10MBMGRB-M (adult-neonatal body mass, gr/age from birth in days) (y) regressed against log10 adult body mass (x). Extant elephants (orange square: L. africana, black dot: E. maximus) are within the lower limit of adult body mass-neonatal body mass GR in ungulates; P. falconeri (red dot) corresponds to the body mass estimation of tibia LTC (Supplementary material 2). (d) Von Bertalanffy growth curves of diaphyseal lengths of the tibiae (TDL) of L. africana (black dots and black curve) and P. falconeri (red dots; black and red curves). P. falconeri growth model 1 (short black curve) is based on ontogenetic data of specimens directly aged by skeletochronology (red dots). The long red curve corresponds to model 2 and is based on the inferred minimal longevity (Table 1; “Materials and methods”) and the maximal value of TDL.

Figure 2

Tibia midshaft sections of P. falconeri. Representation of tissue types in histological sections of an ontogenetic series of tibiae ((a, b, f, e, I, g, k); anterior crest upper); magnifications (c, d, h, j; medullary cavity upper). (a) neonate (T106) showing parts of the birth line; (b, c) (T1): 1 year; longitudinal and radial osteons after the first winter LAG; (d) (T135), (e) (T138): 2.5–3 years ‘Fibro-lamellar complex’ (FLC) with longitudinal, oblique and radial osteons; (f) (T2): 4 years; (g) (T139): 7 years; (h) (T 45): 9 years, still showing active growth (open canals at the outer cortex); (i) (T142): 11 years; (j) (T 203): 22 years, showing an EFS; (k) (Roma6): 23 years;. Zeiss Scope A1 microscope with integrated digital camera (AxioCam ICc5), transmitted light. 10 mm scale: complete sections; 2000 µm scale: magnifications.

Figure 3

Inference of ASM in P. falconeri. (a) Piecewise regressions of tibia diaphyseal lengths (DL) against age (years) in L. africana and P. falconeri. Open black circles and black regression line represent L. africana; large black dot: break point (BP) with its value; open red circles and red regression line correspond to P. falconeri; large red dot: break point (BP) with its value; slopes of regressions are placed over the lines for each taxon (Table 2). (b) Ontogeny of the reproductive phases of L. africana, shown as age-specific conception rates and reproductive activity for a sample of 905 L. africana cows shot in the Krüger National Park (South Africa) between 1970 and 1974, signaling the reproductive ontogenetic phases. Horizontal bar in the upper left corner indicates the timing of the break point (BP) obtained from DL of the tibia with the 95% confidence intervals (See “Materials and methods”; Supplementary material 6). (c) ASM: scatterplot of phylogenetic generalized least square regressions (PGLS) of log ASM (y) against body mass (x) for extant ungulates (n = 145) and elephants (Data base from AnAge). Results of PGLS regression in Supplementary material 8. Blue dots: ungulates; red dot: P. falconeri; green dot: Myotragus balearicus; black dot: Elephas maximus; orange square: L. africana; (d) Residuals of ASM in ungulates from PGLS regression of ASM against body mass. Blue dots: ungulates; Red dot: P. falconeri; Green dot: Myotragus balearicus; Black dot: Elephas maximus; orange square: Loxodonta africana (Data from AnAge Data base).

Figure 4

Tusk growth patterns of P. falconeri. (a) Spinagallo tusks sample analysed. 1: CAT-5; 2: CAT-24; 3: CAT-51; 4: CAT-100; 5: CAT-102; 6: CAT-77-76-78. Graphic scale 5 cm. (Supplementary material 5, Supplementary Table 5). (b) changes in ER over ontogeny (log-transformed age (x) and log of ER (y)) in L. africana and P. falconeri. Blue dots: L. africana females (y = − 0.5116x + 2.291, R² = 0.88); orange dots: L. africana males (y = − 0.3402x + 2.2119, R² = 0.77); red dots: P. falconeri (y = − 0.0446x + 1.0793, R² = 0.22). Observe the low position of the P. falconeri tusk ER regression line and the low exponent, showing the small differences in ER between young and old individuals, which accounts for the stable ontogenetic growth pattern. Green dots L. africana specimens aged by Uno et al.. Black squares correspond to tusks of M. primigenius, M. columbi and M. americanum (c) Box-and-whisker plots comparing the lifespan inferred for P. falconeri (Pf) from the six tusks analysed, with the longevity values of extant elephants (EE) L. africana and H. maximus from AnAge data base, and maximal records of longevity in extant elephants^– (REE); (P) lifespan predicted for P. falconeri from body mass allometry^–; estimations of inferred lifespan for fossil large elephants P. antiquus (Pa) and M. primigenius (Mp). Horizontal lines denote the median, boxes the interquartile range (25–75 percent quartiles), and whiskers the maximum and minimum values; percentile ranks are computed by linear interpolation between the two nearest ranks. (d) Scatterplot of residuals of phylogenetic generalized least square regressions (PGLS) of body mass against longevity from the regression of ungulates (small blue dots); orange square: L. africana (body mass from Anage); black dot: E maximus based on body mass; red dot P. falconeri; green dot M. balearicus from the Pleistocene of the island of Majorca. Results of PGLS regression in Supplementary material 8).

Figure 5

Tusk histology. (a) MicroCT—scan section of P. falconeri tusks. 1: Transversal microCT—scan section of CAT-102 tusk showing dark (winter) light (summer) bands; observe that the winter bands are thinner than summer bands. 2: magnification of (1) showing the last 5 annual incremental bands (pairs of dark–light dentine bands). 3: thin external cementum layer. (b) CAT-24 tusk (slide 24 B2-L1-110305.1) under green fluorescence light (for better visibility of the structures); measurements were taken between daily cross striations to calculate mean daily secretion rate (DSR); white line: prism; the prism was carefully followed as it decussated to estimate the days along the prism between the annual increments; white bars: key annual FOIs; the calculated number of days (white numbers) confirms the annual nature of the increments; Zeiss Scope.A1 microscope fluorescence light. (c) tusk 5 (slide 5-2–4) exemplifies the arrangement of daily increments (parallel green lines) and sub-daily increments (white lines) deposited along the border of the pulp cavity (dark area upper left). (d) CAT 100 tusk with monthly (second-order) increments; red arrow: cementum-dentine junction; (b) green arrows: second-order increments. Zeiss Scope A1 microscope with integrated digital camera (AxioCam ICc5).

Figure 6

Molar growth pattern in P. falconeri. (a) Fragment of lower mandible with the P. falconeri M/3 (CAT-114) used in molar analysis (graphic scale 4 cm); (b) longitudinal section of the posterior part of M/3 (CAT-114) showing the measured plates 8 and 9 (Graphic scale 1 cm); it is still unworn, roots are closed. (c) Growth in plate height plotted against PFT (years) for upper and lower dentition together; black dots: continental elephants (M. columbi; P. antiquus IPS-B1-L1-82167, the last supposed sister taxon of both insular taxa P. cypriotes and P. falconeri); red dots: insular elephants (P. cypriotes, Cyprus; P. falconeri, Sicily). (d) Box-and-whisker plots for PFT of M/3 (red P. falconeri; black L. africana). Mean values correspond to the mean of PFT of the lamellae of the different plates (Supplementary material 7). Horizontal lines denote the median, boxes the interquartile range (25–75 percent quartiles), and whiskers the maximum and minimum values; percentile ranks are computed by linear interpolation between the two nearest ranks. (e) Box-and-whisker plots for EER (mm/y) of the different P. falconeri lamellae and plates studied; EER decreases posteriorly. Horizontal lines denote the median, boxes the interquartile range (25–75 percent quartiles), and whiskers the maximum and minimum values; percentile ranks are computed by linear interpolation between the two nearest ranks (Supplementary material 7).

Figure 7

Molar histology of P. falconeri. (a) Composed slide of the third lower molar (CAT-114, slides IPS 96,003). The tooth is cut horizontally (3 mm lost); it shows the measured plates 8 and 9 (plate 10 was taphonomically heavily cracked and not measurable) with the location of our measurements (green dots). Depending on the state of preservation of each plate, we took 29 measurements on the upper and 25 on the lower half (there are less points because some of them are too close together as to be separated). (b) (slide IPS 85787_3a) illustrates cross striations (blue arrows) along an enamel prism (green), and the enamel-dentine junction (dotted white line) in a lower second molar. (c) unworn Dp4/superior (slide IPS-85040; Supplementary material 7) with green dots signaling location of 16 measurements (there are less points because some of them are too close together as to be separated). Zeiss Scope A1 microscope with integrated digital camera (AxioCam ICc5).

Figure 8

Accumulative bone area in transversal sections of 29 P. falconeri tibiae up to the age of 23 years when growth in bone circumference almost completely ceases. For simplicity, each consecutive annual surface area was calculated including the area of the medullary cavity (see “Materials and methods”). Grey: juveniles that died before onset of puberty; various shades of red and blue: individuals that survived onset of puberty. Individuals older than 15 years (adults) were likely much older than indicated by their last countable LAG because of the almost complete cessation of appositional growth a few years after onset of SM. Thus, for instance, small-sized (probably female) individual 70,096 (Roma6) shows a complete fusion not only of epiphyses but even of tibia and fibula.