El sistema olfatorio de las salamandras (Plethodontidae) y su relación con la detección de depredadores

Ita Andehui Rivera Hernández, Edgar A Bello Sánchez, Laura T Hernández Salazar, Jorge E Morales Mávil

Resumen


Las salamandras de la familia Plethodontidae, ante las presiones de depredación, han tenido que desarrollar diversas estrategias para reducir la probabilidad de un ataque. Las pistas químicas tienen un papel importante en las interacciones depredador-presa. En las salamandras existen dos subsistemas con la capacidad para detectar químicos, el sistema olfatorio principal y el vomeronasal (o sistema accesorio). Se reconoce que la capacidad de detectar e interpretar el reconocimiento de depredadores a partir de estímulos químicos que se pueden encontrar en los sustratos, provoca procesos internos que activan el sistema nervioso autónomo y el sistema endócrino, preparando fisiológicamente a los individuos para dar una respuesta conductual apropiada ante una posible situación de peligro. El eje hipotálamo-hipofisario-adrenal coordina las respuestas adaptativas del organismo a estímulos estresantes, de manera que se activa ante la presencia de un depredador, permitiéndole responder de forma más rápida y eficaz para ajustar la homeostasis y aumentar sus posibilidades de supervivencia. La detección de los depredadores ya sea de manera innata o aprendida, provee a las salamandras de una capacidad de respuesta ante posibles ataques, y muestra la plasticidad neural (memoria olfativa) para mantener almacenada la información o bien, de aprender nueva información, y evocarla cada vez que sea necesaria, para aumentar la eficiencia de la respuesta ante situaciones de peligro. El objetivo de esta revisión es mostrar la información conocida y actualizada de las características morfológicas y fisiológicas de las salamandras pletodóntidas para el reconocimiento de depredadores a través del olfato, como un proceso complejo y vital que involucra distintos componentes, y tiene como finalidad aumentar la probabilidad de éxito de supervivencia de los individuos.

 

Abstract

Salamanders of the Plethodontidae family in the face of predation pressures have had to develop various strategies to reduce the likelihood of an attack. Chemical cues play an important role in predator-prey interactions. In salamanders there are two subsystems with the ability to detect chemicals, the main olfactory system and vomeronasal (or accessory system). It is recognized that the ability to detect and interpret the recognition of predators from chemical stimuli that can be found in substrates causes internal processes that activate the autonomic nervous system and the endocrine system, physiologically preparing individuals to give a behavioral response appropriate to a potentially hazardous situation. The hypothalamic-pituitary-adrenal axis coordinates the adaptive responses of the organism to stressful stimuli, so that it is activated in the presence of a predator, allowing it to respond more quickly and effectively to adjust homeostasis and increase its chances of survival. The detection of predators, either innately or learned, provides salamanders with a capacity to respond to possible attacks, and shows the neural plasticity (olfactory memory) to keep information stored, or learn new information, and evoke it whenever necessary, to increase the efficiency of response to hazardous situations. The aim of this review is to show the known and updated information of the morphological and physiological characteristics of the plethodontid salamanders for the recognition of predators through smell as a complex and vital process that involves different components, and aims to increase the probability of success of survival of individuals.

Keywords: Predator; olfaction; vomeronasal organ; plethodontidae; recognition.


Palabras clave


Depredador; olfato; órgano vomeronasal; plethodontidae; reconocimiento.

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Referencias


Bradbury J., Vehrencamp S. Principles of animal communication. Sinauer Associates, Inc. Massachusetts. 1998 pp 279-318.

Rajchard J. Antipredator pheromones in amphibians: a review. Vet Med-Czech. 2006 51(8): 409-413. Front Neurosci 2013 7: 130.

Meredith M. Sensory processing in the main and accessory olfactory systems: comparisons and contrasts. J. Steroid Biochem. Mol. Biol. 1991 39: 601-614.

Schmidt A, Naujoks-Manteuffel C, Roth G. Olfactory and vomeronasal projections and the pathway of the nervus terminalis in ten species of salamanders. Cell Tissue. Res. 1988 251(1): 45-50.

Thomas RS, Glen DM, Symondson WOC. Prey detection through olfaction by the soil-dwelling larvae of the carabid predator Pterostichus melanarius. Soil Biol. Biochem. 2008 40: 207-216.

Wisenden B D. Olfactory assessment of predation risk in the aquatic environment. Phil. Trans. R. Soc. Lond. 2000 355: 1205-1208.

Apfelbach R, Blanchard CD, Blanchard RJ, Hayes RA, McGregor IS. The effects of predator odors in mammalian prey species: a review of field and laboratory studies. Neurosci. Biobehav. Rev. 2005 29: 1123-1144.

Gillette JR. Odor discrimination in the California slender salamander, Batrachoseps attenuatus: evidence for self-recognition. Herpetologica 2002 58: 165-170.

Placyk Jr JS, Graves BM. Foraging behavior of the red-backed salamander (Plethodon cinereus) under various lighting conditions. J. Herpetol. 2001 35: 521-524.

Marvin GA, Davis K, Dawson J. Effect of acute low body temperature on predatory behavior and prey-capture efficiency in a plethodontid salamander. Physiol Behav. 2016 158:121-127.

Telfer AC, Laberge F. Responses of Eastern red-backed salamanders (Plethodon cinereus) to chemical cues of prey presented in soluble and volatile forms. Physiol Behav 2013 115:6-13.

Davis DR, Gabor CR. Behavioral and physiological antipredator responses of the San Marcos salamander, Eurycea nana. Physiol Behav 2015 139: 145-9.

Wells K. The ecology and behavior of amphibians. The University of Chicago Press. Chicago 2007 417 - 418.Stress and depression-induced immune dysfunction: implications for the development and progression of cancer. INT REV PSYCHIATR 2005 17: 515-27.

Lima S, Dill L. Behavioral decisions made under the risk of predation – a review and prospectus. Can J Zool. 1990 68: 619–640.

Brodie, Jr. ED. Antipredator adaptations of salamanders: Evolution and convergence among terrestrial species. En: Margaris, NS, Arianoutsou-Faraggitaki A and Reiter RJ. Plant, animal, and microbial adaptations to terrestrial environment. Plenum Publishing Corp. 1983 109-133. ¿CLIN CHILD FAM PSYCH 2005 8: 89-105.

Kuchta S, Krakauer A, Sinervo B. Why does the Yellow-eyed Ensatina have yellow eyes? Batesian mimicry of Pacific newts (genus Taricha) by the salamander Ensatina eschscholtzii xanthoptica. Evolution 2008 62: 984-990.

Toledo L, Sazima I, Haddad C. Behavioural defences of anurans: an overview. Ethol Ecol Evol. 2011 23: 1 - 25.

Caldwell P, Thorp JH, Jervey TO. Predator-prey relationships among larval dragonflies, salamanders and frogs. Oecologia 1980 46: 285-289.http://apps.who.int/iris/bitstream/10665/43770/1/9789243591650_spa.pdf

Crane A, McGrane C, Mathis A. Behavioral and physiological responses of ozark zigzag salamanders to stimuli from an invasive predator: the armadillo. Int J Ecol. 2012 2012: 1-7.

Sullivan A, Madison D, Rohr J. Behavioural responses by red-backed salamanders to conspecific and heterospecific cues. Behaviour 2003 140: 553-564.

Sullivan A, Madison D, Rohr J. Variation in the antipredator responses of three sympatric plethodontid salamanders to predator-diet cues. Herpetologica 2004 60(4): 401-408.

Ferrari MC, Brown GE, Messier F, Chivers DP. Threat-sensitive generalization of predator recognition by larval amphibians. Behav Ecol Sociobiol. 2009 63(9): 1369-1375.

Ferrari MC, Wisenden BD, Chivers DP. Chemical ecology of predator–prey interactions in aquatic ecosystems: a review and prospectus. The present review is one in the special series of reviews on animal–plant interactions. Can J Zool. 2010 88(7): 698-724.

Ferrari MC, Messier, F, Chivers DP. First documentation of cultural transmission of predator recognition by larval amphibians. Ethology 2007 113(6): 621-627.

Marvin G, Whitekiller R, Hutchison V. Avoidance of alarm chemicals by plethodontid salamanders (Genus Eurycea): Importance of Phylogeny, Ecology, and Methodology. Herpetologica 2004 60(1): 24-33.

Chivers DP, Ferrari MC. Social learning of predators by tadpoles: does food restriction alter the efficacy of tutors as information sources? Anim Behav. 2014 89: 93-97. Biol Psychol 2016.

Ferrari MC, Vrtělová J, Brown GE, Chivers DP. Understanding the role of uncertainty on learning and retention of predator information. Compar. Cogn. 2012 15(5): 807-813.

Ferrari MC, Brown GE, Bortolotti GR., Chivers DP. Linking predator risk and uncertainty to adaptive forgetting: a theoretical framework and empirical test using tadpoles. Proc R Soc. Lond. B Biol Sci. 2010: 2205-2210.

Nevitt GA. Olfactory foraging by antarctic procellariiform seabirds: life at High Reynolds numbers. Biol Bull. 2000 198: 245-253.

Placyk Jr JS, Graves BM. Prey detection by vomeronasal chemoreception in a plethodontid salamander. J Chem Ecol. 2002 28: 1017-1036.

Catania KC, Hare JF, Campbell KL. Water shrews detect movement, shape, and smell to find prey underwater. Proc Nat Acad Sci. 2008 105: 571-576.

Chivers DP, Smith RJF. Free-living fathead minnows rapidly learn to recognize pike as predators. J Fish Biol. 1995 46:949-954.

Madison DM, Maerz JC, McDarby JD. Chemosensory avoidance of snake odors by salamanders: freeze and flight contingencies. En: Johnston RE, Müller-Schwarze D, Sorensen P. Advances in chemical communication in vertebrates. Kluwer Academic/Plenum Press 1999 508-516.

Dawley E M, Bass A H. Chemical access to the vomeronasal organs of a plethodontid salamander. J Morphol. 1989 200 (2): 163-174.

Vitt L, Caldwell J. Herpetology. An introductory biology of amphibians and reptiles. Academic Press China 2014 70-71.

Buck L. Axel R. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 1991 65: 175-187.

Laberge F, Hara TJ. Neurobiology of fish olfaction: a review. Brain Res Rev. 2001 36: 46- 59.

Dawley E, Bass A. Organization of the vomeronasal organ in a plethodontid salamander. J Morphol. 1988 198: 243 - 255.

Dawley EM. Correlation of salamander vomeronasal and main olfactory system anatomy with habitat and sex: behavioral interpretations. En: Doty RL, Müller-Schwarze. Chemical Signals in Vertebrates VI. Plenum Press 1992 403-409.

Tsigos C, Chrousos G. Hypothalamic–pituitary–adrenal axis, neuroendocrine factors and stress. J Psychosom Res. 2002 53: 865 - 871.

Dennis JC, Aono S, Vodyanoy J, Morrison ED. Development, morphology, and functional anatomy of the olfactory epithelium. En: Handbook of olfaction and gustation (Ed. R.L. Doty). Publisher John Wiley & Sons, Inc. 2015 93-121.

Kandel ER, Schwartz JH, Jessell TM, Agud JL. Principios de neurociencia. McGraw-Hill Interamericana, Madrid. 2001 pp 625-633.

Laberge F, Roth G. Connectivity and cytoarchitecture of the ventral telencephalon in the salamander Plethodon shermani. J Comp Neurol. 2005 482(2): 176-200.

Laberge F, Mühlenbrock-Lenter S, Grunwald W, Roth G. Evolution of the amygdala: new insights from studies in amphibians. Brain Behav Evol. 2006 67(4): 177-187.

Amaral DG. The amygdala, social behavior, and danger detection. Ann NY Acad Sci. 2003 1000(1): 337-347.

Davis M. The role of the amygdala in fear and anxiety. Annu Rev Neurosci. 1992 15: 353-75.

Martínez S. Eje hipotálamo-hipofisario-adrenal. En: Martínez S. Hormonas, Estado de ánimo y función cognitiva. Publicaciones Delta. 2007 41-51.

Matteri R, Carrol J, Dyer C. Neuroendocrine responses to stress. En: Moberg G y Mench J. The biology of animal stress. Basic principles and implications for animal welfare. CABI publishing 2000 43-76.

Boyd, T., McGoldrick, J., Michanowicz, A., Thomas, R. Chemosensory adaptation in antipredator responses of common Pennsylvania salamanders. J Ecol Res. 2006 8: 9-14.

Sullivan A, Maerz J, Madison D. Anti-predator response of red-backed salamanders (Plethodon cinereus) to chemical cues from garter snakes (Thamnophis sirtalis): laboratory and field experiments. Behav Ecol Sociobiol. 2002 51: 227–233.




DOI: https://doi.org/10.25009/eb.v8i19.2530

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