Eye and Skin Differences between Atelognathus patagonicus Morphotypes: Two Environments, Two Strategies (Anura; Batrachylidae)
The adults of the frog Atelognathus patagonicus display phenotypic plasticity and two morphotypes, namely, “aquatic” and “littoral”, and the transition from one to the other is a reversible way of adapting to different environments. The aquatic form lives underwater associated with vegetation and rocks and has lateral skin folds and interdigital membranes. Otherwise, the littoral form lives up to a few kilometers away from the water and does not have bagginess and the interdigital membranes are reduced. Considering that morphology and function of the visual system and skin composition are characters highly associated with habitat conditions, we performed a histological comparison of the eye and skin of both aquatic and littoral morphotypes of A. patagonicus. The aquatic morphotype A. patagonicus does not have an evident character that improves vision underwater, suggesting that clues for subaquatic life could not be only visual. However, the eyelid of the littoral morph has more mucous glands than that of the aquatic morph, which is consistent with the mucus secretion of these glands and its association with terrestrial environments. Also, the skin littoral morph is more keratinized and thicker than the aquatic one, which helps to prevent desiccation. Finally, the lateral skin of the aquatic morph is highly vascularized, suggesting an increase in cutaneous respiration. This work is a starting point for understanding, in an integrative way, the different mechanisms and systems modifications in the water–land transition of A. patagonicus.ABSTRACT
Photographs of adults of Atelognathus patagonicus. (A) Aquatic morphotype. (B) Littoral morphotype. Observe that the aquatic form possesses lateral skin folds (bagginess) and the interdigital membranes (arrow) well developed, whereas the littoral form has no bagginess and the interdigital membranes are reduced (arrow).
(A) Sagittal section of the eye from an adult of littoral Atelognathus patagonicus (MMT). (B) Detail of retina and choroid (PAS-H). (C) Detail of umbraculum (hematoxylin and eosin [H&E]). (D) Protein content in the lens (CB). Note the weak reaction in neural retina and the connective tissue of the cornea. Asterisk: rod external segment. Bm = Bruch's membrane; c = cornea; ce = corneal epithelium; ch = choroid; es = external segments; gc = ganglion cell; i = iris; ie = iris epithelium; in = inner nuclear layer; ip = inner plexiform layer; is = iris stroma; l = lens; le = lower eyelid; nm = nictitating membrane; nr = neural retina; on = outer nuclear layer; op = outer plexiform layer; pr = pigmented retina; sc = scleral cartilage; sp = substantia propria of the cornea; ti = tunica interna; tf = tunica fibrosa; tv = tunica vasculosa; u = umbraculum; ue = upper eyelid; v = blood vessel.
(A) Sagittal section of the upper eyelid of aquatic Atelognathus patagonicus showing gland distribution (H&E). (B) Detail of the edge of the eyelid with only mucous glands (MMT). (C) Neutral GAGs in mucous and serous glands (PAS-H). (D) Acidic GAGs in mucous but not in serous glands (AB-H). (E) Protein content in mucous and serous glands (CB). (F) Sagittal section of the lower eyelid of aquatic A. patagonicus showing gland distribution (H&E). Inset: PAS-H stain of mucous gland in nictitating membrane. Black arrowhead: mucous gland; white arrowhead: serous gland. b = basal membrane; d = dermis; e = epidermis; m = melanophores; v = blood vessel.
Number of mucous and serous glands in the superior eyelid of littoral (black bar) and aquatic (white bar) morphotypes. Results are expressed as the mean of 10 eye sections ± SE. Asterisk indicates significant differences between morphotypes.
Transversal sections of dorsal skin of Atelognathus patagonicus. Because there are no differences between morphotypes for these characters, the photographs were chosen for the better representation of the characters. (A) General aspect of a littoral representative (MMT). (B–D) Histochemistry techniques were as follows: (B) PAS-H (aquatic representative), (C) AB-H (littoral representative), and (D) CB (aquatic representative). Black arrowhead: mucous gland; white arrowhead: serous gland.
Transversal sections of lateral skin of Atelognathus patagonicus. Because there are no differences between morphotypes for histochemical properties, the photographs were chosen for the better representation of the characters. (A) General aspect of an aquatic representative (MMT). (B–D) Histochemistry techniques were as follows: (B) PAS-H (littoral representative), (C) AB-H (aquatic representative), and (D) CB (aquatic representative). Black arrowhead: mucous gland; white arrowhead: serous gland.
Transversal sections of ventral skin of Atelognathus patagonicus. Because there are no differences between morphotypes for these characters, the photographs were chosen for the better representation of the characters. (A) General aspect of a littoral representative (MMT). (B–D) Histochemistry techniques were as follows: (B) PAS-H (aquatic representative), (C) AB-H (littoral representative), and (D) CB (aquatic representative). Black arrowhead: mucous gland; white arrowhead: serous gland.
Comparison of mucous glands (A), serous glands (B), and capillaries (C) in dorsal, lateral and ventral skin areas between littoral (black bar) and aquatic (white bar) morphotypes. For all cases, results are expressed as the mean of 10 skin sections ± SE. Asterisks indicate significant differences between morphotypes.
Transversal section of lateral skin from aquatic morph of Atelognathus patagonicus. (MMT). Black arrowhead: mucous gland; c = capillary; dcl = dermis compact layer; dsl = dermis soft layer; m = melanophore; v = vessel.
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