Vertebrate florivory of vascular epiphytes: the case of a bromeliad / Florivores vertebrados de epífitas vasculares: o caso de uma bromélia

Abstract The avoidance of vertebrate herbivory is thought to be one of the possible drivers for the evolution of epiphytism. Scarce literature suggests that epiphyte herbivory is mainly related to insect attack on reproductive structures. In a pine-oak forest we observed almost all inflorescences of an epiphytic bromeliad (Tillandsia carlos-hankii) with signs of florivory; the degree of damage suggested that vertebrate herbivores could be involved. To assess the intensity of vertebrate florivory damage we recorded the percentage of damaged individuals in a 500 m2 plots during two flowering seasons. To identify possible vertebrate herbivores, we installed 20 mixed capture stations, 10 photo-traps focused on bromeliads and analyzed stomach contents of captured vertebrates. Florivory was observed on 62% of individuals during the first flowering season and 77% on the second; and average one individual lost 41% of reproductive structures. Vertebrates associated with florivory were a bird, Icterus bullockii (Aves, Passeriformes, Icteridae), a squirrel Sciurus aureogaster (Mammalia, Rodentia, Sciuridae), and mice, Peromyscus gratus, P. levipes and P. aztecus (Mammalia, Rodentia, Cricetidae). Our results suggest that vascular epiphytes are used as opportunistic resources for small vertebrates during seasons when preferred resources are scarce.

Resumo Acredita-se que a prevenção da herbivoria dos vertebrados é um dos possíveis impulsores da evolução da epífita. A literatura escassa sugere que a herbivora em epífitas está relacionada principalmente ao ataque de insetos as estruturas reprodutivas. Em uma floresta de pinheiros observamos que quase da todas as inflorescências de uma bromélia epífita (Tillandsia carlos-hankii) apresentavam sinais de florivoria; o grau de danos sugeria que herbívoros majores (vertebrados) pudessem estar envolvidos. Para avaliar a intensidade do dano de florivoria de vertebrados, registramos a porcentagem de indivíduos danificados em quadrantes de 500 m2 durante duas estações de florescimento. Para identificar possíveis herbívoros vertebrados, instalamos 20 estações de captura mista e analisamos o conteúdo estomacal de vertebrados capturados. Além disso, foram instaladas 10 foto-armadilhas focadas em bromélias. A florivoria foi observada em 62% dos indivíduos durante a primeira estação de floração e 77% na segunda. Os vertebrados associados à florivoria foram pássaro, Icterus bullockii (Aves, Passeriformes, Icteridae), um esquilo Sciurus aureogaster (Mammalia, Rodentia, Sciuridae) e ratos, Peromyscus gratus, P. levipes e P. aztecus (Mammalia, Rodentia, Cricetidae). Assim, nossos resultados sugerem que epífitas vasculares são usadas como recurso facultativo para estes animais durante as estações, quando os recursos preferidos estão escassos.

Vertebrate florivory of vascular epiphytes: the case of a bromeliad

Abstract The avoidance of vertebrate herbivory is thought to be one of the possible drivers for the evolution of epiphytism. Scarce literature suggests that epiphyte herbivory is mainly related to insect attack on reproductive structures. In a pine-oak forest we observed almost all inflorescences of an epiphytic bromeliad (Tillandsia carlos-hankii) with signs of florivory; the degree of damage suggested that vertebrate herbivores could be involved. To assess the intensity of vertebrate florivory damage we recorded the percentage of damaged individuals in a 500 m2 plots during two flowering seasons. To identify possible vertebrate herbivores, we installed 20 mixed capture stations, 10 photo-traps focused on bromeliads and analyzed stomach contents of captured vertebrates. Florivory was observed on 62% of individuals during the first flowering season and 77% on the second; and average one individual lost 41% of reproductive structures. Vertebrates associated with florivory were a bird, Icterus bullockii (Aves, Passeriformes, Icteridae), a squirrel Sciurus aureogaster (Mammalia, Rodentia, Sciuridae), and mice, Peromyscus gratus, P. levipes and P. aztecus (Mammalia, Rodentia, Cricetidae). Our results suggest that vascular epiphytes are used as opportunistic resources for small vertebrates during seasons when preferred resources are scarce.

Resumo Acredita-se que a prevenção da herbivoria dos vertebrados é um dos possíveis impulsores da evolução da epífita. A literatura escassa sugere que a herbivora em epífitas está relacionada principalmente ao ataque de insetos as estruturas reprodutivas. Em uma floresta de pinheiros observamos que quase da todas as inflorescências de uma bromélia epífita (Tillandsia carlos-hankii) apresentavam sinais de florivoria; o grau de danos sugeria que herbívoros majores (vertebrados) pudessem estar envolvidos. Para avaliar a intensidade do dano de florivoria de vertebrados, registramos a porcentagem de indivíduos danificados em quadrantes de 500 m2 durante duas estações de florescimento. Para identificar possíveis herbívoros vertebrados, instalamos 20 estações de captura mista e analisamos o conteúdo estomacal de vertebrados capturados. Além disso, foram instaladas 10 foto-armadilhas focadas em bromélias. A florivoria foi observada em 62% dos indivíduos durante a primeira estação de floração e 77% na segunda. Os vertebrados associados à florivoria foram pássaro, Icterus bullockii (Aves, Passeriformes, Icteridae), um esquilo Sciurus aureogaster (Mammalia, Rodentia, Sciuridae) e ratos, Peromyscus gratus, P. levipes e P. aztecus (Mammalia, Rodentia, Cricetidae). Assim, nossos resultados sugerem que epífitas vasculares são usadas como recurso facultativo para estes animais durante as estações, quando os recursos preferidos estão escassos.

Effects of natural environmental conditions on the ovarian histometric dynamics of five striped squirrels (Funambulus pennanti) / Efectos de las condiciones ambientales naturales sobre la dinámica histométrica de ovarios en la ardilla de las palmeras (Funambulus pennanti)

The present study was designed to determine the morphological and histological variations in the female palm squirrel's reproductive organs which inhabit croplands of central Punjab. 16 specimens were collected from 3 different locations of Faisalabad district during different months in order to collect their ovaries samples in order to determine the breeding phenology of this species. Body weight and external body measurements were recorded. Two adult females were autopsied each month and their ovaries were extracted. Tissue were prepared by the tissue paraffin technique and stained by H&E. Seasonal variations in the follicular size and shape were observed. Statistical analysis revealed that values of all parameters of ovaries were significantly (P<0.01) higher during peak folliculogenic phase (January to May) as compared to low folliculogenic phase (November­December). Three reproductive phases were observed according to follicular development i.e., quiescent period (November- December), recrudescence period (January) and peak reproductive phase (February­March). In conclusion of this study, different phases of sexual activities are determined which are controlled by seasonal variations. These variations are in accordance to different physical factors which influences gross anatomical and histological changes of ovaries and folliculogensis of female five-striped northern palm squirrel (Funambulus pennanti) for adjustments in breeding phenology.

El presente estudio fue diseñado para determinar las variaciones morfológicas e histológicas en los órganos reproductores de la ardilla de las palmeras que habita en las tierras de cultivo del centro de Punjab. Dieciséis muestras fueron recolectadas en 3 lugares diferentes del distrito de Faisalabad durante diferentes meses con el fin de obtener los ovarios y determinar la fenología reproductiva de esta especie. Se registraron el peso corporal y las medidas corporales externas. Se realizaron autopsias de dos hembras adultas cada mes y sus ovarios fueron extraídos. Se prepararon los tejidos por técnica de parafina y tinción H & E y se observaron las variaciones estacionales en el tamaño y forma folicular. El análisis estadístico reveló que los valores de todos los parámetros de los ovarios fueron significativamente más altos durante la fase foliculogénica (enero a mayo), en comparación con la fase baja (noviembre-diciembre) (P <0,01). De acuerdo al desarrollo folicular se observaron tres fases reproductivas, el período de reposo (noviembre-diciembre), el período de recrudecimiento (enero) y la fase peak reproductiva (febrero-marzo). En conclusión las diferentes fases de las actividades sexuales definitivamente están controladas por variaciones estacionales. Estas variaciones se ajustan a diferentes factores físicos que influyen en los cambios anatómicos e histológicos de los ovarios y la folículogénesis de la ardilla hembra de las palmeras (Funambulus pennanti) para realizar ajustes en la fenología de su reproducción.

The Kidney and Adrenal Gland of the African Palm Squirrel Epixerus ebii: A Microanatomical Observation / El Riñón y la Glándula Adrenal de la Ardilla de la Palma Africana Epixerus ebii: Una Observación Microanatómica

The kidneys and adrenal glands of the African palm Squirrel (Epixerus ebii), were subjected to histological and mucin histochemical studies. The kidney was covered by a capsule of periodic acid of shiff (PAS) positive connective tissue fibres. The kidney parenchyma was composed of large peripheral cortex and smaller centrally placed medulla. The cortex contained renal corpuscle, proximal convoluted tubules, distal convoluted tubules and juxtaglomerullar complex. At the hilus, the renal artery and vein, ureters, and nerve fibres were surrounded by adipose tissue. The renal medullar was composed of Henles’ loop and collecting ducts. The adrenal gland cortex contained zona glomerulosa, zona fasciculate and zona reticulata. The zona fasciculata was the largest of the zones containing polyhedrally shaped cells with less basophilic nuclei and very foamy cytoplasm. Some cells of zona fasciculate were binucleated. The adrenal medulla contained mostly glandular cells, few ganglion cells and capillaries. This study establishes that the organs investigated are typical of mammals. It will fill the knowledge gap, help wildlife clinicians in disease diagnosis of these organs in this species.

Los riñones y las glándulas adrenales de la ardilla de la Palma Africana (Epixerus ebii) fueron objeto de estudios histológicos y de estudios histoquímicos con mucina. El riñón estaba cubierto por una cápsula de fibras de tejido conectivo que resultaron positivas a la coloración con ácido peryódico de Schiff (PAS). El parénquima renal estaba constituido por una gran corteza periférica y una médula más pequeña, ubicada centralmente. La corteza contenía el corpúsculo renal, los túbulos contorneados proximales, los túbulos contorneados distales y un complejo yuxtaglomerular. A nivel del hilio del órgano, la arteria y vena renales, los uréteres y las fibras nerviosas estaban rodeados de tejido adiposo. La médula renal estaba compuesta por el asa de Henle y los túbulos colectores. La corteza de la glándula adrenal contenía las zonas glomerular, fasciculada y reticular. La zona fasciculada era la mayor de las tres y contenía células con forma poliédrica con núcleos menos basofilícos y citoplasma muy esponjoso. Algunas células de la zona fasciculada eran binucleadas. La médula adrenal contenía principalmente células glandulares y pocas células ganglionares y capilares. Los resultados de este estudio establecieron que los órganos investigados son típicos de los mamíferos. Esta investigación llenará la brecha de conocimiento existente y ayudará a los clínicos de fauna silvestre en el diagnostico de enfermedades de estos órganos en esta especies.

Histology of the parotid salivary gland of the african palm squirrel (epixerus ebii) / Histología de la glándula parótida salival de la ardilla de la palma africana (epixerus ebii)

The parotid salivary gland microscopic morphology of the adult African Palm squirrel (Epixerus ebii) was investigated. This study was carried out to provide the basic histology of this organ in the palm squirrel, as there is dearth of information of its microscopic morphology from available literature. This becomes more important as the increasing use of this species of rodent as a pet and animal of importance in African game reserves for tourist attraction. The possibility of its domestication as a ready source of animal protein is also growing. Hence the need to understand the digestive biology to help animal nutritionist in feed formulation. The histology revealed the presence of only serous secretory acini cells. The serous cells were triangular to polyhedral shaped with a roundish basally located nucleus inside the mostly pinkish granulated cytoplasm. Myoepithelial cells were seen around the secretory cells and the intercalated ducts. The intralobular ducts of intercalated and striated ducts were lined by simple cuboidal and simple columnar cells, respectively. The excretory duct seen in the surrounding connective tissue was lined by stratified cuboidal cells. The granules in the cytoplasm of serous cells must be the digestive enzyme amylase that initiates carbohydrate digestion. This well developed serous parotid salivary gland reflects the need for efficient carbohydrate digestion since the animal forages on fruits and nuts that are rich in carbohydrates. The granules could also contain lysozymes which serve in local defense against pathogenic agents in the oral cavity. This study for the first time documents the normal histology of the parotid salivary gland in this species, hence filling the knowledge gap that will help biologists to investigative more profundly. It will also help wild life veterinarians in diagnosis disease.

Se investigó la histología de la glándula parótida salival de la ardilla adulta de la palma Africana (Epixerus ebii). Este estudio se realizó para proporcionar la histología básica de este órgano en esta especie animal, ya que hay escasez de información relacionada con su morfología microscópica proveniente de la literatura disponible. Esto constituye un aspecto importante, por el incremento en el uso de esta especie de roedor como mascota y como animal de importancia en las reservas animales africanas de atracción turística. También está creciendo la posibilidad de su domesticación como una fuente rápida de proteína animal. De allí, la necesidad de entender la biología digestiva para ayudar al nutricionista en la formulación alimenticia. Los resultados de los estudios histológicos solamente revelaron la presencia de células acinares secretoras serosas. La forma de las células serosas varió de triangular a poliédrica, con un núcleo redondeado, localizado basalmente dentro de un citoplasma granulado predominantemente rosáceo. Se observaron células mioepiteliales alrededor de las células secretoras y de los ductos intercalados. Los ductos intralobulares de los ductos intercalados y estriados estaban alineados respectivamente en células cúbicas simples y en células columnares simples. El ducto excretor observado en el tejido conectivo circundante estaba alineado por células cúbicas estratificadas. Los gránulos en el citoplasma de las células serosas pudieran corresponderse con la enzima amilasa que inicia la digestión de carbohidratos. Esta glándula salival parótida bien desarrollada, refleja la necesidad de una eficiente digestión de carbohidratos, ya que el animal se alimenta de frutos y nueces ricos en estos principios inmediatos. Los gránulos también pudieran contener lisozimas que sirven para la defensa contra agentes patógenos presentes en la cavidad oral. Este estudio documenta por primera vez, la histología normal de la glándula parótida de esta especie, llenando por consiguiente, la brecha de conocimiento que ayudará a los biólogos a investigar más profundamente, y a los veterinarios que trabajan en fauna silvestre, en el diagnóstico de enfermedades.