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The Parotoid Macroglands in Rhinella Marina and Rhaebo Guttatus PEDRO L

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The Parotoid Macroglands in Rhinella Marina and Rhaebo Guttatus PEDRO L RESEARCH ARTICLE Passive and Active Defense in Toads: The Parotoid Macroglands in Rhinella marina and Rhaebo guttatus PEDRO L. MAILHO‐FONTANA1, MARTA M. ANTONIAZZI1, LUÍS F. TOLEDO2, VANESSA K. VERDADE3, JULIANA M. SCIANI1, KATIA C. BARBARO1, DANIEL C. PIMENTA1, 4 1 MIGUEL T. RODRIGUES , AND CARLOS JARED * 1Instituto Butantan, São Paulo, Brazil 2Museu de Zoologia, Universidade Estadual de Campinas, Campinas, Brazil 3Centro de Ciências Naturais e Humanas, Universidade Federal ABC, Santo André, Brazil 4Departamento de Zoologia, Universidade de São Paulo, São Paulo, Brazil ABSTRACT Amphibians have many skin poison glands used in passive defense, in which the aggressor causes its own poisoning when biting prey. In some amphibians the skin glands accumulate in certain regions forming macroglands, such as the parotoids of toads. We have discovered that the toad Rhaebo guttatus is able to squirt jets of poison towards the aggressor, contradicting the typical amphibian defense. We studied the R. guttatus chemical defense, comparing it with Rhinella marina,a sympatric species showing typical toad passive defense. We found that only in R. guttatus the parotoid is adhered to the scapula and do not have a calcified dermal layer. In addition, in this species, the plugs obstructing the glandular ducts are more fragile when compared to R. marina.As a consequence, the manual pressure necessary to extract the poison from the parotoid is twice as high in R. marina when compared to that used in R. guttatus. Compared to R. marina, the poison of R. guttatus is less lethal, induces edema and provokes nociception four times more intense. We concluded that the ability of R. guttatus to voluntary squirt poison is directly related to its stereotyped defensive behavior, together with the peculiar morphological characteristics of its parotoids. Since R. guttatus poison is practically not lethal, it is possibly directed to predators' learning, causing disturbing effects such as pain and edema. The unique mechanism of defense of R. guttatus may mistakenly justify the popular myth that toads, in general, squirt poison into people's eyes. J. Exp. Zool. 9999A: XX–XX, 2013. © 2013 Wiley Periodicals, Inc. How to cite this article: Mailho‐Fontana PL, Antoniazzi MM, Toledo LF, Verdade VK, Sciani JM, J. Exp. Zool. Barbaro KC, Pimenta DC, Rodrigues MT, Jared C. 2013. Passive and active defense in toads: The 9999A:1–13, 2013 parotoid macroglands in Rhinella marina and Rhaebo guttatus. J. Exp. Zool. 9999:1–13. Grant sponsor: CAPES and CNPq‐INCTTox—Brazilian Federal Government. ÃCorrespondence to: Carlos Jared, Cell Biology Laboratory, Instituto The skin of amphibians is characterized by the presence of mucous Butantan, Av. Vital Brasil 1500, CEP 05503‐000 São Paulo, Brazil. glands, mainly associated with protection against desiccation, and E‐mail: [email protected] granular glands, or poison glands, associated with chemical Received 8 July 2013; Revised 6 September 2013; Accepted 13 defense against predators and microorganisms (Toledo and September 2013 Jared, '95; Hillman et al., 2009). DOI: 10.1002/jez.1838 Published online XX Month Year in Wiley Online Library In some species the poison glands are grouped into large and (wileyonlinelibrary.com). very conspicuous protuberances, such as the parotoid macroglands © 2013 WILEY PERIODICALS, INC. 2 MAILHO‐FONTANA ET AL. of toads (Toledo and Jared, '95; Duellman and Trueb, '96; the interdisciplinary nature of this work, biochemical and Clarke, '97; Jared et al., 2009). These macroglands are located in pharmacological studies on the parotoid secretion of both species the post‐orbital region and, on the skin surface, can be identified by were also carried out. The poison of R. guttatus showed low the presence of large pores from which the poison is ejected toxicity when compared to that of R. marina. However, it causes (Hostetler and Cannon, '74; Toledo et al., '92; Toledo and Jared, '95; high levels of inflammation and pain. All data were analyzed in Almeida et al., 2007; Jared et al., 2009). The parotoids are light of the natural history and the differences in the defensive constituted by many alveoli formed by a resistant collagenous behavior of the two species. connective tissue. The alveolar disposition side by side gives the appearance of honeycomb to the whole assembly (Jared et al., 2009). Each alveolus bears a very large poison gland that MATERIALS AND METHODS communicates with the outside through a duct lined by a thick Animals epithelial tissue forming a plug, which obstructs the duct and Six adult male R. marina (Fig. 1a) with snout‐vent length (SVL) avoids poison release, acting as a cork in a bottle (Jared (114.91 Æ 2.67 mm) and six adult Rhaebo guttatus (Fig. 1c) (SVL et al., 2009). 115.52 Æ 11.3mm) were respectively collected in Santarém and When toads are disturbed, they inflate the lungs and assume a Jacareacanga, state of Pará, Brazil. Male Swiss mice, weighing 18– stereotyped posture, offering the parotoids to the aggressor 20 g, were used in pharmacological experiments. All animal (Toledo and Jared, '95; Jared et al., 2009; Toledo et al., 2011). The procedures were performed in accordance with the standards of parotoids then, due to the internal pressure coming from the lungs, the Ethics Committee on Animal Use of Instituto Butantan become very turgid and ready to trigger poisonous shots in case (CEUAIB) (protocol #837/11). any external mechanical pressure is exerted, such as the bite of an aggressor (Jared et al., 2009). The abrupt pressure exerted by the Behavior bite is transferred to the alveoli leading to the rupture of the To obtain behavioral data, the animals were gently stimulated epithelial plugs and causing the expulsion of the poison in the in their natural environment, using a twig or a finger. This form of jets (Jared et al., 2009). Therefore, it is the predator who procedure followed the protocol of Toledo et al. (2011), applied causes its own poisoning, which can often be lethal (Sakate and in other behavioral studies and does not cause any harm to the Lucas de Oliveira, 2000; Jared and Antoniazzi, 2009; Jared toads. et al., 2009). Predator's self‐poisoning is characteristic of amphibian defense, which is classified as a “passive defense” Morphology (Jared and Antoniazzi, 2009; Antoniazzi et al., 2013), as opposed The animals were euthanized with a lethal dose of thiopental and to “active defense” presented, for example, by the snakes, who fixed in Bouin or 4% formaldehyde for histology and scanning attack the aggressor and inject their venom through glands electron microscopy (SEM), or in Karnowsky ('65), for transmis- compressed by surrounding muscles (Kochva, '78; Pough sion electron microscopy (TEM). et al., 2001; Jared et al., 2009). For anatomical examination of the fixed animals, the parotoids In Brazil, toads are represented by seven genera, Rhinella being were carefully detached from the dorsal skin for observation of the most representative. Rhinella marina is one of the most studied their relationship with the surrounding bones, muscles, and other toads, distributed from Texas, in North America, to the center of tissues. South America, in the Brazilian Amazon (Frost, 2013). Its defense For histology, fragments of dorsal skin and parotoids of both is typically passive, possessing well‐developed parotoids covering species were embedded in paraffin following routine histological almost the entire central part of the dorsal region. Another procedures. The scapular girdle of R. guttatus was also prepared common bufonid genus in the Amazonian region and Central following the same methods after decalcification in 4% ethyl- America is Rhaebo, from which the species R. guttatus is enediamine tetraacetic acid (EDTA) for 3 months. The sections of all widespread throughout the Brazilian Amazon. Recently it was samples (2‐ to 6‐mm thick) were stained with hematoxylin–eosin, reported that the defensive behavior of this species opposes to that Picrosirius or von Kossa (Bancroft and Steven, '90; Junqueira et al., found in other bufonids and other anurans in general. In contrast '79). The images were obtained by an Olympus BX51 microscope to the characteristic passive defense of amphibians, R. guttatus, and captured through a digital camera using the software Image‐ when disturbed, displays a series of stereotypical postures that Pro Express from MediaCybernetics (Rockville, MD, USA). surprisingly culminate with the voluntary ejection of its poison For SEM, fragments of the parotoids were dried in vacuum, towards the aggressor, at distances of up to 2 m (Jared et al., 2011). mounted in stubs and analyzed under low vacuum in a FEI Quanta The aim of this work was the comparative morphological study 250 microscope. For TEM, fragments of the parotoids were post‐ of the parotoids and their associated structures in the two toads in fixed in 1% osmium tetroxide, contrasted in 1% uranyl acetate order to understand the structural differences that lead to the and embedded in epoxy resin. Ultrathin sections were examined in voluntary ejection of poison in R. guttatus. Taking advantage of a LEO 906E microscope. J. Exp. Zool. PAROTOID MACROGLANDS AND DEFENSE IN TOADS 3 Figure 1. (a) Adult specimen of Rhinella marina. The arrow indicates the parotoid pores. (b) Manual compression upon the parotoid of R. marina mimetizing the pressure exerted by the bite of a predator. (c) Adult specimen of Rhaebo guttatus. The arrow indicates the parotoid pores. (d) Voluntary ejection of poison through the parotoid of R. guttatus.(e–g) Sequence of behavioral defensive postures of R. guttatus culminating with poison squirting upwards (g). Skin Secretion HPLC system (20A Prominence, Shimadzu Co., Kyoto, Japan). The parotoid secretion from eight specimens of R. marina and R. Aliquots of 20 mL of the secretions were loaded in a C18 column guttatus was obtained by manual compression of the macrog- (ACE C18, 5 mm, 100 A, 250 mm  4.6 mm) in a two‐solvent lands (Fig.
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