Resumen de Estudio microtomográfico de la anatomía funcional de dos especies de insectos plaga, el psílido asiático de los cítricos, diaphorina citri (hemiptera liviidae) y la broca del café, hypothenemus hampei (coleoptera, curculionidae)
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RESUMEN Tradicionalmente, el estudio de la anatomía interna en los insectos, se ha basado en técnicas de disección con las limitaciones propias de la misma. La microtomografía computarizada (micro-CT), es una técnica relativamente nueva que se basa en la obtención de imágenes de rayos X que tras ser procesadas permite reconstruir la anatomía externa e interna y del espécimen. Así como separar con diferente color las estructuras. Pudiendo observarlas en su posición anatómica desde cualquier perspectiva y sin necesidad de realizar disecciones y por tanto sin las deformaciones y destrucción que estas implican. Todo ello ha abierto un abanico de posibilidades inimaginables antes, e imposibles, con los métodos clásicos de disección y/o con las técnicas de microscopía.
El objetivo principal de esta tesis doctoral ha sido realizar un estudio microtomográfico detallado (con imágenes 3D de alta resolución y vídeos) de la anatomía externa e interna de dos especies de insectos plaga: el psílido asiático de los cítricos (Diaphorina citri Kuwayama, 1908) y la broca del café (Hypothenemus hampei Ferrari, 1867), de gran importancia a nivel mundial por los enormes daños y pérdidas económicas que provocan. Adicionalmente, durante la realización del estudio de la actividad de H. hampei en el interior de la cereza del café, encontramos especímenes del gorgojo del grano de café (Araecerus fasciculatus De Geer en 1775) emergiendo de las cerezas del café, este descubrimiento motivó un estudio del mismo y su actividad dentro de la cereza del café, que fue objeto de una publicación adicional al respecto y que se incluye como material adicional.
Los resultados aquí obtenidos, junto con los del trabajo previo (en que realizamos un estudio microtomográfico de la abeja de la miel y comparamos los resultados con la publicación clásica de Snodgrass sobre la anatomía de la especie), confirman que las técnicas de micro-CT constituyen una excelente alternativa a los métodos tradicionales basados en la disección. Al ser una técnica no destructiva que permite observar las estructuras (externas e internas) en su posición anatómica real, desde cualquier perspectiva, tantas veces como se requiera, sin riesgo de deformarlas o romperlas. Y sin los inconvenientes de las deformaciones producidas durante las manipulaciones que requiere la disección. Asimismo, durante el estudio microtomográfico de ambas especies se ha podido completar detalles de estructuras ya descritas por otros autores y al mismo tiempo se han descubierto otras que nunca habían sido descritas, y que de no ser por la micro-CT difícilmente podrían haberse puesto de manifiesto. Los resultados obtenidos, en su mayor parte ya publicados, de una forma resumida han sido los siguientes: El psílido asiático de los cítricos (Diaphorina citri): Anatomía externa (la cabeza, con descripción detallada de las estructuras, incluidos el aparato bucal, ojos y antenas; el tórax, morfología de los diferentes segmentos, patas, escleritos, distribución de los espiráculos, y las alas; el abdomen -segmentos, distribución de los espiráculos, y terminalia de ambos sexos-). Anatomía interna (digestivo, faringe, esófago, cámara filtradora, intestino medio, e intestino posterior y ano; sistema excretor, las estructuras tubulares –apéndices- del intestino medio, consideradas clásicamente como túbulos de Malpigio; estructuras internas de la cámara cibarial (bomba precibarial -salivar-, bomba cibarial, conos maxilares y mandibulares y los músculos asociados; disposición de los estiletes, glándulas -salivares, coxales y antenales-, las glándulas coxales y antenales se describen y citan por vez primera en Psylloidea, discutiéndose su posible función como productoras de feromonas sexuales; sistema traqueal -espiráculos, y disposición de los tubos traqueales abdominales-; sistema circulatorio -vaso dorsal, aorta y músculos aliformes-; sistema nervioso -cerebro, cadena nerviosa ganglionar ventral y nervios-, se describen por vez primera en Psylloidea la existencia de diferencias sexuales en la conformación del cerebro y ganglios de la cadena nerviosa ventral; sistema reproductor masculino -testículos, vesículas seminales, glándulas accesorias, bomba espermática, conductos de conexión y edeago-; sistema reproductor femenino -ovarios, glándulas accesorias, espermateca, glándula coleterial/cementante, conductos de conexión y el ovipositor-, la anatomía funcional de la espermateca se describe y analiza por primera vez en Psylloidea; bacterioma -situación, organización externa e interna-; siendo la primera reconstrucción tridimensional del mismo; diferentes detalles de la musculatura). Aspectos anatómico-morfológicos y funcionales derivados de la alimentación picadora-chupadora (estructuras implicadas, punto de perforación, los estiletes dentro de los vasos de la planta y las vainas salivares.) La broca del café (Hypothenemus hampei): Estudio de la actividad vital de H. hampei en el interior de la baya del café (se observó, un patrón comportamental en el que la hembra se coloca con el abdomen dirigido al exterior, taponando la entrada de los túneles. Asimismo, la construcción de túneles presenta un trazado en zig-zag que dificulta la penetración de posibles parasitoides. Por otro lado el aprovechamiento de los recursos alimenticios de la cereza del café se maximiza gracias a la secuencia constructora de los túneles y cámaras de oviposición. Que de forma secuencial comienza en la periferia semilla y se mueve hacia el interior). Anatomía externa (la cabeza -estructuras y diferencias sexuales en número y disposición de omatidios-; el tórax -diferentes segmentos, espiráculos respiratorios y primera observación sobre las diferencias sexuales en la morfología del pronoto-; el abdomen -espiráculos respiratorios, y diferencias sexuales en el número de segmentos-.Anatomía interna (aparato digestivo -esófago, buche, proventrículo, intestino medio, intestino posterior, ciegos gástricos, ampolla rectal y ano, se describen por primera vez diferencias sexuales en la conformación y número de circunvoluciones del intestino medio; sistema excretor -número y disposición de los túbulos de Malpigio-; sistema reproductor masculino -testículos, glándulas accesorias, vesículas seminales, bomba espermática, conducto eyaculador y primera descripción del edeago-; sistema reproductor femenino -ovarios, oviductos laterales, glándula accesoria, espermateca, glándula espermática, oviducto común y gonoporo-; sistema respiratorio -con un detallado estudio de los espiráculos respiratorios; se describen por vez primera, en detalle, los sistemas de filtración que presentan, y se reconstruye por vez primera todo el sistema de tubos traqueales, nombrándose las diferentes ramas, algunas nunca antes descritas. Habiéndose calculado la longitud total de tubos y estudiado la distribución por tamaños de la luz interna- ; aparato circulatorio -vaso dorsal y aorta-; sistema nervioso -cerebro, ganglios de la cadena nerviosa ventral y nervios, se describen por vez primera diferencias sexuales en el tamaño y conformación del cerebro-; la musculatura -señalando por vez primera una reducción de los músculos implicados en el vuelo en los machos-.
El gorgojo del grano de café (Araecerus fasciculatus): La especie fue descrita en 1775 como Curculio fasciculatus, y es la primera vez en los dos siglos y medio transcurridos en que gracias a las modernas técnicas de microtomografía se ha podido "congelar" la actividad del insecto en el interior de una baya de café y estudiarla en detalle. Este estudio ha revelado aspectos interesantes de la biología del gorgojo del café dentro de la baya del café. Habiéndose reconstruido larvas de 5º estadio y hembras dentro de la cereza del café. Además, durante el estudio se descubrió un ejemplar macho de una especie no descrita de coleóptero de la familia Ptinidae (Ptinus s.tr. sp.)
- English
ABSTRACT Traditionally, the study of the internal anatomy of insects has been based on dissection techniques with their own limitations. The computerized microtomography (micro-CT), is a relatively new technique that is based on obtaining X-ray images that after being processed allows to reconstruct the external and internal anatomy and the specimen, as well as to separate with different color the structures. Being able to observe them in their anatomical position from any perspective and without the need for dissections and therefore without the deformations and destruction that these imply. All this has opened up a range of possibilities previously unimaginable, and impossible, with the classic methods of dissection and/or microscopy techniques.
The main objective of this doctoral thesis has been to carry out a detailed microtomographic study (with high resolution 3D images and videos,) of the external and internal anatomy of two species of insect pests: the Asian citrus psyllid (Diaphorina citri Kuwayama, 1908) and the coffee berry borer (Hypothenemus hampei Ferrari, 1867), of great importance worldwide due to the enormous damage and economic losses they cause. Additionally, during the study of H. hampei's activity within the coffee cherry, we found specimens of the coffee bean weevil (Araecerus fasciculatus De Geer in 1775) emerging from coffee cherries. This discovery motivated a study of the bean weevil and its activity within the coffee berry, which was the object of an additional publication on the subject and which is included as additional material.
The results obtained here, together with those of our previous work (in which we carried out a microtomographic study of the honey bee and compared the results with the classic publication of Snodgrass on the anatomy of the species), confirm that the micro-CT techniques constitute an excellent alternative to the traditional methods based on dissection. As it is a non-destructive technique that allows to observe the structures (external and internal) in their real anatomical position, from any perspective, as many times as required, without the risk of deforming or breaking them. And without the inconvenience of the deformations produced during the manipulations required for dissection. Likewise, during the microtomographic study of both species it has been possible to corroborate structures already described by other authors and at the same time others have been discovered, never described before, which if it were not for the micro-CT could hardly have been made evident. The results obtained, for the most part already published, in a summarized form, have been the following:
The Asian Citrus Psyllid (Diaphorina citri): External anatomy (the head, with detailed description of the structures, including the oral system, eyes and antennae; the thorax, morphology of the different segments, legs, sclerites, distribution of the spiracles, and the wings; the abdomen -segments, distribution of the spiracles, and terminalia of both sexes-). Internal anatomy (digestive, pharynx, esophagus, filter chamber, midgut, and hindgut and anus; excretory system, the tubular structures -appendices- of the midgut, classically considered as Malpigium tubules; internal structures of the cibarial chamber (precibarial -salivary - pump, cibarial pump, maxillary and mandibular cones and associated muscles; stylets bundle, glands -salivary, coxal and antennal-, coxal and antennal glands are described and cited for the first time in Psylloidea, discussing their possible function as producers of sexual pheromones; tracheal system -spiracles, and disposition of the abdominal tracheal tubes-; circulatory system -dorsal vessel, aorta and aliform muscles-; Nervous system -brain, ventral ganglion nerve chain and nerves-, the existence of sexual differences in the conformation of the brain and ventral ganglion nerve chain are described for the first time in Psylloidea; male reproductive system -testicles, seminal vesicles, accessory glands, spermatic pump, connection ducts and edeagus-; female reproductive system -ovaries, accessory glands, spermatheca, colleterial/cement gland, connecting ducts and the ovipositor-, the functional anatomy of the spermatheca is described and analyzed for the first time in Psylloidea; bacteriome -situation, external and internal organization-; being the first three-dimensional reconstruction of it; different details of the musculature). Anatomical-morphological and functional aspects derived from the chopper-sucker feeding (structures involved, perforation point, the stylets inside the plant vessels and the salivary sheaths).
The coffee berry borer (Hypothenemus hampei): Study of the vital activity of H. hampei inside the coffee berry (a behavioral pattern was observed in which the female is placed with the abdomen directed to the outside, blocking the entrance of the tunnels. Likewise, the construction of tunnels presents a zig-zag pattern that makes the penetration of possible parasites difficult. On the other hand, the use of the food resources of the coffee cherry is maximized thanks to the construction sequence of the tunnels and oviposition chambers. That in a sequential way begins in the seed periphery and moves towards the interior). External anatomy (the head - structures and sexual differences in the number and arrangement of ommatidia; the thorax - different segments, respiratory spiracles and first observation on sexual differences in the morphology of the pronotum; the abdomen - respiratory spiracles, and sexual differences in the number of segments. Internal anatomy (digestive system -esophagus, crop, proventricle, midgut, hindgut, gastric cecum, rectal ampulla and anus-, sexual differences in the conformation and number of circumvolutions of the midgut are described for the first time; excretory system -number and arrangement of Malpigio's tubules-; male reproductive system -testes, accessory glands, seminal vesicles, spermatic pump, ejaculatory duct and first description of the edeagus-; female reproductive system - ovaries, lateral oviducts, accessory gland, spermatheca, spermatic gland, common oviduct and gonopore; respiratory system - with a detailed study of the respiratory spiracles; the filtering systems they present are described for the first time in detail, and the whole system of tracheal tubes is reconstructed for the first time, naming the different branches, some of them never described before. Having calculated the total length of the tubes and studied the distribution of internal light by size, the circulatory system -dorsal and aortic vessels-; the nervous system -brain, ventral nerve chain nodes and nerves, sexual differences in the size and shape of the brain are described for the first time; the musculature -showing for the first time a reduction in the muscles involved in flight in males-.
The Coffee Bean Weevil (Araecerus fasciculatus): The species was described in 1775 as Curculio fasciculatus, and this is the first time in the two and a half centuries since then that thanks to modern microtomography techniques it has been possible to "freeze" the insect's activity inside a coffee berry and study it in detail. This study has revealed interesting aspects of the biology of the bark beetle inside the coffee berry. Having reconstructed 5th instar larvae and females inside the coffee berry. In addition, during the study a male specimen of an undescribed species of beetle from the family Ptinidae (Ptinus s.tr. sp.) was discovered.
Bibliografía más relevante utilizada en la tesis Alba-Alejandre, I., Alba-Tercedor, J., & Vega, F. E. (2019). Anatomical study of the coffee berry borer (Hypothenemus hampei) using micro-computed tomography. Scientific Reports, 9(17150), 1–16. https://doi.org/10.1038/s41598-019-53537-z Alba-Alejandre, I., Hunter, W. B., & Alba-Tercedor, J. (2018). Micro-CT study of male genitalia and reproductive system of the Asian citrus psyllid, Diaphorina citri Kuwayama, 1908 (Insecta: Hemiptera, Liviidae). PLoS ONE, 13(8), 1–11. https://doi.org/https://doi.org/10.1371/journal.pone.0202234 Editor: Alba-Tercedor, J. (2013). Study of the anatomy of the common housefly Musca domestica Linnaeus, 1758 (Insecta: Diptera, Muscidae) scanned with the Skyscan 1172 high resolution micro-CT. Bruker Micro-CT Users Meeting 2013, 275–289.
Alba-Tercedor, J., & Alba-Alejandre, I. (2019). Comparing micro-CT results of insects with classical anatomical studies: The European honey bee (Apis mellifera Linnaeus, 1758) as a benchmark (Insecta: Hymenoptera, Apidae). Microscopy and Analysis, 3(1), 12-15 EU. Retrieved from https://microscopy-analysis.com/article/january_19/comparing_classical_anatomical_studies_of_insects Alba-Tercedor, J., Alba-Alejandre, I., & Vega, F. E. (2019). Revealing the respiratory system of the coffee berry borer (Hypothenemus hampei; Coleoptera: Curculionidae: Scolytinae) using micro-computed tomography. Scientific Reports, 9(17753), 1–17. https://doi.org/10.1038/s41598-019-54157-3 Alba-Tercedor, J., & Bartomeus, I. (2016). Micro-CT as a tool straddling scientist research, art and education. Study of Osmia sp., a mason bee (Insecta, Hymenoptera: Megachilidae). In Bruker Micro-CT Users Meeting 2016 (pp. 74–91).
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