Trophic specialisation reflected by radular tooth material properties in an "ancient" Lake Tanganyikan gastropod species flock

Abstract

Background: Lake Tanganyika belongs to the East African Great Lakes and is well known for harbouring a high proportion of endemic and morphologically distinct genera, in cichlids but also in paludomid gastropods. With about 50 species these snails form a flock of high interest because of its diversity, the question of its origin and the evolutionary processes that might have resulted in its elevated amount of taxa. While earlier debates centred on these paludomids to be a result of an intralacustrine adaptive radiation, there are strong indications for the existence of several lineages before the lake formation. To evaluate hypotheses on the evolution and radiation the detection of actual adaptations is however crucial. Since the Tanganyikan gastropods show distinct radular tooth morphologies hypotheses about potential trophic specializations are at hand.

Results: Here, based on a phylogenetic tree of the paludomid species from Lake Tanganyika and adjacent river systems, the mechanical properties of their teeth were evaluated by nanoindentation, a method measuring the hardness and elasticity of a structure, and related with the gastropods' specific feeding substrate (soft, solid, mixed). Results identify mechanical adaptations in the tooth cusps to the substrate and, with reference to the tooth morphology, assign distinct functions (scratching or gathering) to tooth types. Analysing pure tooth morphology does not consistently reflect ecological specializations, but the mechanical properties allow the determination of eco-morphotypes.

Conclusion: In almost every lineage we discovered adaptations to different substrates, leading to the hypothesis that one main engine of the flock's evolution is trophic specialization, establishing distinct ecological niches and allowing the coexistence of taxa.

Keywords: Adaptive radiation; Functional morphology; Gastropoda; Mechanical properties; Nanoindentation; Trophic specialisation.

Fig. 1

Shells of examined species. Black scale bars: from Lake Tanganyika. Blue scale bar: from adjacent river systems. Forms next to the letters a–x indicate preferred feeding substrate (circle = mud, hexagon = sand, square = plants, triangle = rock). a Bridouxia ponsonbyi ZMB 220.137-1, b B. grandidieriana BMNH 1889.6.23.57-61, c B. rotundata ZMB 220.063-3, d B. praeclara DBL 19-4, e Spekia zonata ZMB 220.007-2, f Leloupiella minima ZMB 220.008-3, g Reymondia horei ZMB 220.007-1, h Cleopatra johnstoni ZMB 220.102, i Stanleya neritinoides ZMB 102.624-1, j  Tanganycia rufofilosa ZMB 102.621-1, k Martelia tanganyicensis ZMB 220.134-1, l Anceya giraudi ZMB 220.000-1, m Syrnolopsis lacustris ZMB 220.046-1, n Chytra kirki SMF 290543-1, o Limnotrochus thomsoni SMF 290542-1, p Tiphobia horei SMF 290550-1, q Paramelania iridescens SMF 290,538, r P. damoni SMF 290531-2, s P. crassigranulata SMF 290528-1, t Mysorelloides multisulcata DBL without number, u Lavigeria spinulosa ZMB 220114, v L. grandis SMF 292827-1, w L. nassa ZMB 220.172-1, x L. livingstoniana ZMB 220116; Scale bars: a–d, f, k, l, m = 2.5 mm; e = 5 mm; g, i, j, n, o, v, w = 10 mm; h = 5 mm; p–s = 20 mm, t = 0.75 mm; u, x = 6 mm

Fig. 2

a Schematic drawing of the radula when feeding, b Taenioglossan radula of Spekia zonata (ZMH 150008/999-2), black line = area of nanoindentation for central, lateral, and marginal teeth, c Radula (ZMB220.143-2) embedded in epoxy resin and polished for nanoindentation (longitudinal section along the radula) with (d–f) magnification of some tested areas (e with nanoindentation mark; f crosses indicate points of indentation), g Representative results as nanoindentation measurement curves for basis, stylus, and cusps of central teeth (Young’s modulus, GPa, versus displacement into tooth material). The values for the cusps within the indentation depth of 480–520 nm were used for further calculation. Scale bars: b = 100 µm; c = 250 µm; d, e = 30 µm; f = 60 µm. CT central tooth, FP food particle, FZ formation zone, IMT inner marginal tooth, IRT immature radular teeth, LT lateral tooth, MRT mature radular teeth, O odontophore, OMT outer marginal tooth, RM radular muscles, RT radular teeth, WZ working zone

Fig. 3

Radular teeth of: a, b  Bridouxia ponsonbyi ZMB 220.137-1, a overview, b marginals; c, d B. grandidieriana ZMB 220.139-4, c overview, d centrals and laterals; e, f B. rotundata ZMB 220063-1, e overview, f marginals; g, h B. praeclara ZMB 220.063-2, g overview, h marginals. Scale bars: a = 40 μm; b, d, f, h = 10 μm; c, e, g = 20 μm. Forms indicate preferred feeding substrate (circle = mud, hexagon = sand, square = plants, triangle = rock)

Fig. 4

Radular teeth of: a, b Spekia zonata ZMH 150008/999-2, a overview, b marginals; c, d Leloupiella minima ZMB 220.135, c overview, d marginals; e, f Reymondia horei ZMB 220.147-1, e centrals and laterals, f marginals; g, h Cleopatra johnstoni ZMB 220.102-1, g overview, h marginals. Scale bars: a = 100 μm; b = 50 μm; c, d = 10 μm; e, f = 30 μm; g = 40 μm; h = 20 μm. Forms indicate preferred feeding substrate (circle = mud, hexagon = sand, square = plants, triangle = rock)

Fig. 5

Radular teeth of: a, b Stanleya neritinoides MRAC without number, a centrals and laterals, b marginals; c, d Tanganycia rufofilosa, c centrals and laterals, d marginals; e, f Martelia tanganyicensis ZMB 220.133-1, e overview, f laterals and marginals; g, h. Anceya giraudi ZMB 220.132, g overview, h centrals and laterals. Scale bars: a–c, e, f, h = 10 μm; d, g = 30 μm. Forms indicate preferred feeding substrate (circle = mud, hexagon = sand, square = plants, triangle = rock)

Fig. 6

Radular teeth of: a, b Syrnolopsis lacustris ZMB 220.131, a overview, b marginals; c, d Chytra kirki IRSNB no. 63, c overview, d centrals and laterals; e, f Limnotrochus thomsoni ZMB 107.102, e overview, f centrals and laterals; g, h Paramelania iridescens ZMB 220.053, g overview, h centrals. Scale bars: a = 30 μm; b, h = 10 μm; c = 100 μm; d, f = 20 μm; e = 50 μm; g = 120 μm. Forms indicate preferred feeding substrate (circle = mud, hexagon = sand, square = plants, triangle = rock)

Fig. 7

Radular teeth of: a, b Paramelania damoni ZMH without number, a centrals and laterals, b marginals; c, d P. crassigranulata ZMB 220.037-1, c overview, d centrals and laterals; e, f Mysorelloides multisulcata IRSNB no. 126, e centrals and laterals, f marginals; g, h Lavigeria spinulosa ZMB 220.051, g overview, h marginals. Scale bars: a, f = 10 μm; b, d, h = 30 μm; c, g = 100 μm; e = 20 μm. Forms indicate preferred feeding substrate (circle = mud, hexagon = sand, square = plants, triangle = rock)

Fig. 8

Radular teeth of: a, b Lavigeria grandis ZMH 154657/999, a overview, b laterals and marginals; c, d L. nassa ZMB 220.074, c overview, d laterals and marginals; e, f L. livingstoniana ZMB 220.117-1, e overview, f marginals and laterals. Scale bars: a = 100 μm; b = 50 μm; c, d, f = 30 μm; e = 100 μm. Forms indicate preferred feeding substrate (circle = mud, hexagon = sand, square = plants, triangle = rock)

Fig. 9

Results of nanoindentation, hardness (GPa) and Young’s modulus (GPa). (left) Comparing all tooth cusps of species feeding on mixed, soft, and solid substrate; (right) comparing all central to all lateral and all marginal tooth cups. Letters are connecting letters from Tukey–Kramer test. N = quantity of tested tooth cusps

Fig. 10

Results of nanoindentation. Hardness (GPa) and Young’s modulus (GPa) for all cusps (central, lateral, marginal, with N = quantity of measured cusps) for each species (N = quantity of measured specimens) correlated with the preferred feeding substrate (circle = mud, hexagon = sand, square = plants, triangle = rock). Connecting letters from Tukey–Kramer test can be found in Table 1

Fig. 11

Results of nanoindentation. Median of Young’s modulus (GPa) of the central, lateral, and marginal tooth cusps for each species correlated with the preferred feeding substrate (circle = mud, hexagon = sand, square = plants, triangle = rock) against the background of a phylogenetic tree (Bayesian). Taxa without molecular information were allocated to groups based on morphological analyses from relevant literature. Reconstructed ancestral feeding substrate of the lower taxonomic levels is plotted next to the nodes

Fig. 12

Changes of Young’s modulus over the phylogeny (excl. outgroups) visualized using continuous character mapping (from 5 GPa [blue] to 10 GPa [red]) for a central tooth, b lateral tooth, c marginal tooth for the lower taxonomic levels