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Feeding ecomorphology of seven demersal marine fish species in the Mexican Pacific Ocean

How fish functional morphology shapes species co-existence and assemblage diversity patterns is a fundamental issue in ecological research. In fishes, much is known about the ecomorphological relationships of feeding morphology in coral reef fishes and in freshwater taxa inhabiting distinct environments. However, little is known about the patterns and processes shaping morphological variation in other oceanic taxa; particularly those inhabiting soft bottom habitats. In this study, we assessed patterns of feeding ecomorphology in seven demersal teleost species associated with soft bottoms of the continental shelf in the central Mexican Pacific Ocean. Feeding analyses indicated that some species groups shared similar diets. Likewise, patterns of morphological variation based on geometric morphometrics demonstrated that some taxa did not differ in body shape, while patterns of variation in other species were seen in body length and height, caudal peduncle height and the anal fin anterior insertion point. A multivariate association between diet composition data and overall body shape indicated significant    ecomorphological    relationships,    describing   a   continuum

between species displaying benthopelagic morphology and specializing on prey with high speed swimming ability (Engraulidae), versus species with benthic morphology and specializing on fast escape prey (crustacea). The clear ecomorphological patterns observed for these seven species at both the individual and species levels imply that environmental conditions and resource availability allow these taxa to differentially inhabit and exploit the soft bottom ecosystem. Fish diversity is principally represented by the benthic morphology, although benthopelagic morphology, also show a high degree of success in this environment.

2015. Bohórquez-Herrera, J., V. H. Cruz-Escalona, D.C. Adams & M.S. Peterson. Feeding ecomorphology of seven demersal fish species in the Mexican Pacific Ocean. Environmental Biology of Fishes , 98 (1): Published online first. DOI: 10.1007/s10641-014-0373-1

Plasticity in the agonistic behaviour of male California sea lions, 
Zalophus californianus

Environmental conditions may influence mating behaviour in otariids breeding in areas with elevatedtemperatures and intense solar radiation. Although they have evolved morphological and physiologicaladaptations to prevent overheating while breeding on land, under extreme temperature conditions, theymust adjust their behaviour in order to thermoregulate. The California sea lion mating system is based onmale competition and displays that occur while defending their territories when females are present.Westudied the agonistic behaviour of adult males at two breeding colonies in Mexico with contrastingenvironmental characteristics: Isla Santa Margarita (ISM) (Pacific coast) and Isla San Esteban (ISE) (Gulfof California). The goal of this study was to determine which variables influence where (i.e. on land or inthe water) aggressive interactions between adult males occurred using logistic regression analysis. Weanalysed three scenarios: (1) both islands, (2) only ISM and 

(3) only ISE. The best model for the firstscenario included the air temperature, density of females and type of aggression. The second scenarioinvolved the density of females, and the third scenario included the rate of female interactions. Althoughthe California sea lion mating strategy involves monopolizing critical resources, our results indicate thatdensity of females and rate of female interactions have a significant impact on where male aggressiveinteractions occur. Our results highlight how changing environmental conditions affect the behaviouralplasticity of this species’ mating system. Most notably, males inhabiting high-temperature environmentsuse the thermoregulatory strategy of defending territories adjacent to the coast while remainingimmersed in the water. This strategy may result in decreased polygyny in the Gulf of California coloniesrelative to those on the Pacific coast.

2014. Bohórquez-Herrera, J., C.J. Hernández-Camacho, D. Aurioles-Gamboa & V. Cruz-Escalona. Plasticity in the agonistic behaviour of male California sea lions, Zalophus californianus. Animal Behaviour, 89: 31-38.

Foraging behavior delays mechanically-stimulated escape responses in fish

Foraging and the evasion of predators both are fundamental for the survival of organisms, but they impose contrasting demands that can influence performance in each behavior. Previous studies suggested that foraging organisms may experience decreased vigilance to attacks by predator; however, little is known about the effect of foraging on escape performance with respect to the kinematics and the timing of the response. The present study tested the hypothesis that engaging in foraging activities affected escape performance by comparing fast-start escape responses of silver-spotted sculpins Blepsias cirrhosus under three conditions: (1) control (no foraging involved), (2) while targeting prey and (3) immediately after capture of prey. 

Escape response variables (non-locomotor and locomotor) were analyzed from high-speed videos. Responsiveness was lower immediately after capturing a prey item compared to the other two treatments, and latency of performance was higher in the control treatment than in the other two. Locomotor variables such as maximum speed, maximum acceleration, and turning rates did not show statistical differences among the three groups. Our results demonstrate that foraging can negatively affect two fundamental components of the escape response, (1) responsiveness and (2) latency of escape, suggesting that engaging in foraging may decrease an individual’s ability to successfully evade predators.

2013. Bohórquez-Herrera, J., S.W. Kawano & P. Domenici. Foraging behavior delays mechanically-stimulated escape responses in fish. Integrative and Comparative Biology, published online. doi: 10.1093/icb/ict031.

Diet composition of batoids on the continental shelf off Nayarit and Sinaloa, Mexico

Since elasmobranchs are frequently apex predators in marine ecosystems, information on their diet is essential for understanding trophic relationships in these systems. Trophic similarity between six batoid species (Rhinoptera steindachneri, Rhinobatos glaucostigma, Dasyatis dipterura, Urotrygon aspidura, U. nana, and U. rogersi) was examined by analyzing the stomach contents of 140 individuals. Specimens were caught by the commercial shrimp fishery in the central Mexican Pacific. In total, 88.6% of the stomachs were completely to partially full, allowing the identification of 77 types of prey. The primary dietary components were crustaceans, followed by annelids and mollusks. Values of diet breadth for the six species indicated low diversity in prey items. Diet similarity suggested two trophic guilds: R. glaucostigma, U. nana, and U. aspidura belong to the cancritrophic guild (P < 0.05) and U. rogersi and D. dipterura to the annelid crustacean guild. Rhinoptera steindachneri showed no evident pattern of association (feeding primarily on ophiuroids). In light of these results, we argue that a distribution of alimentary resources (niche partitioning) between the six species favors their coexistence.

2012. Navarro-González, J. A., J. Bohórquez-Herrera, A.F. Navia & V. Cruz-Escalona. Diet composition of batoids on the continental shelf off Nayarit-Sinaloa, Mexico. Ciencias Marinas, 38(2): 347-362.

Guía para la identificación de especies de tiburones, rayas y quimeras de Colombia

Los tiburones, rayas y quimeras son especies acuáticas agrupadas en la Clase Condrictios, caracterizadas por tener esqueleto de cartílago, escamas placoideas y órganos copuladores externos en los machos (llamados cláspers). Estos animales ocupan diversos ambientes tanto marinos, como estuarinos y dulceacuícolas, y diversas zonas, desde la zona tropical a las zonas polares. En Colombia, varias especies de tiburones y rayas pueden ser observadas in situ en diversos ambientes, teniendo los mismos un gran valor ecológico y turístico. Así mismo, muchos de ellos (incluyendo las quimeras) son susceptibles de ser capturados en diversas pesquerías, teniendo algunos de ellos valor comercial y otros siendo simplemente descartados por carecer del mismo.

De cualquier forma, Colombia, considerado un país megadiverso tanto por las flora como por la fauna acuática y terrestre, lo es así mismo por la diversidad de especies de condrictios, contando con 126 especies confirmadas para las áreas marinas y dulceacuícolas de Colombia, correspondientes a 63 especies de tiburones, 60 de rayas y 3 de quimeras.

Esta guía está dirigida tanto a la comunidad en general, con miras a divulgar la biodiversidad de este grupo de animales en nuestro país, así como a estudiantes, investigadores, observadores, pescadores, administradores locales y regionales pesqueros y ambientales que desarrollan diversas actividades relacionadas con los condrictios. Así, se espera aportar en el adecuado aprovechamiento y manejo de estos recursos, como parte integral del Plan de Acción Nacional para la conservación y manejo de tiburones, rayas y quimeras de Colombia (PAN-Tiburones), liderado por la autoridad pesquera, INCODER.

2011. Tobón-López, A., J. Bohórquez-Herrera, M.A. Tobón & H. Bent-Hooker. Familia Myliobatidae. In:​​​ ​​​​​Guía para la identificación de especies de tiburones,​​​​​​​​​​​​​​​rayas y quimeras de Colombia (Eds. Mejía-Falla, P.A., A.F. Navia & V. Puentes)​​​​​​​.​​​​​​​Bogotá, D.C., Colombia: Ministerio de ​​Ambiente y Desarrollo Sostenible; Corporación para el Desarrollo ​Sostenible del Archipiélago de San Andrés, Providencia y Santa ​Catalina – CORALINA; Gobernación de San Andrés, Providencia y ​Santa Catalina, Fundación SQUALUS, 2011. p. 11-19.​​​

Phylogenetic and ecological components of the morphological variation in mammals skulls (Ph.D. candidature exam)

El cráneo de los mamíferos es una estructura de naturaleza compleja que acarrea excelente información sobre la filogenia y la ecología de las especies; proporcionando un excelente sistema para realizar estudios que involucren la integración morfológica a escalas macro evolutivas. Por esta razón, este ensayo buscó exponer las relaciones que tiene tanto la historia evolutiva representada en la filogenia de las especies; como los aspectos ecológicos en la forma del cráneo de los mamíferos. 

La determinación certera de las relaciones filogenéticas de los mamíferos ha mostrando grandes discrepancias entre la información genética y morfológica; sin embargo, información reciente provee información que permite sugerir dos momentos  de  diversificación  de  especies:  el  primero  se  dio  en  la  barrera

Cretácico/Triásico (K/T) después del evento de extinción masiva; seguido por un segundo momento de diversificación, hace aproximadamente 33 Ma, como una probable respuesta al inicio de la glaciación en la Antártica y a la expansión de praderas. La evolución de los mamíferos ha estado caracterizada por la modificación de sus estructuras anatómicas, para el desarrollo de complejas estructuras. Durante este proceso, los mamíferos​ desarrollaron múltiples modificaciones craneales destacándose el desarrollo del oído medio,​el cierre mandibular y la evolución de los molares tribosfénicos. A pesar de la complejidad de algunos arreglos ecomorfológicos craneales y mandibulares; la historia evolutiva de este grupo muestra convergencias iterativas a lo largo del tiempo, demostrando que algunos fenómenos evolutivos surgen como respuesta a condiciones similares.

Desde el punto de vista filogenético, se ha demostrado que existe una relación compleja entre la cercanía filogenética, la integración y la función; sobre la definición de las formas del cráneo de los mamíferos a lo largo de la evolución. La probabilidad de comprobar la influencia de la historia evolutiva en la morfología craneal de los organismos, se incrementa cuando se analizan niveles taxonómicos bajos o cuyas secuencias de divergencia moleculares son pequeñas; contrario a cuando se analizan grupos más lejanos con divergencias mayores. El cráneo de los mamíferos es una estructura cuya morfología puede verse influenciada por factores externos durante la ontogenia de los individuos; como resultado de los ajustes evolutivos y ecológicos entre el fenotipo y el ambiente. Evolutivamente en los mamíferos el hábitat ha sido una de las principales fuentes de variación morfológica, mostrando especializaciones complejas para especies que viven o pasan partes de sus ciclos de vida en ambientes acuáticos, terrestres y aéreos.

La dieta es sin duda otro de los factores que ha determinado la evolución del tamaño, forma y robustez del cráneo y mandíbula, al igual que la forma, el tamaño y la disposición de los dientes; proporcionando especializaciones específicas para cada tipo de dieta. La morfología craneal también parece estar respondiendo a las conductas de agresión entre machos, como un mecanismo de ofensa, defensa, y para sus exhibiciones ritualísticas frente a las hembras. Análisis preliminares, muestran que el lobo marino de California muestra una relación entre la forma del cráneo y la conducta de agresión entre los machos adultos, mostrando que los individuos cuyas peleas las desarrollan sobre la playa con golpes en cabeza y cuello, tienen cráneos más cortos y robustos, con cajas craneanas de mayor tamaño; de manera opuesta a aquellos cuyas luchas se desarrollan en el agua.

2011. Bohórquez-Herrera, J. Componentes filogenéticos y ecológicos de la variación morfológica del cráneo de mamíferos. Ph.D. candidature exam. Centro Interdisciplinario de Ciencias Marinas, Instituto Politécnico Nacional. La Paz, B.C.S., México. 49 p.

Feeding ecomorphology of  some fishes species associated with soft bottoms (M.Sc. Thesis)

Ecomorphology is a discipline that studies the interactions between morphological and ecological diversity, and explains how individual morphological variation will lead to functional and performance differences. In this study, we analyze the trophic ecomorphology of some fishes species captured as by-catch in the shrimp trawl fishery associated with the soft bottoms of the Nayarit continental shelf during the 2006-2007 fishing season. We used seven species that had taxonomical identification, the diet characterized and were comparable using the same morphometric protocol (Selene peruviana, Lutjanus guttatus, Orthopristis chalceus, Pomadasys panamensis, Centropomus robalito, Pseudupeneus grandisquamis and Polydactylus opercularis). The trophic spectrum was analyzed by the numerical, gravimetric and occurrence frequency indices, as well asstatistical tools and ordination techniques; identifying some species groups that share similar trophic spectrums: ichthyophagous, carcinoicthyophagous, carcinophagous and omnivorous. 

These species’s morphology was analyzed using a geometric morphometric technique which allows extraction of shape information, keeping the geometric relations of the fishes shape, and enhances the results with graphical visualization and interpretation of the morphological variation. Other statistical and ordination techniques were also used, showing that Lutjanidae and Haemulidae species did not present significant differences in their shape, while patterns of variation in other species were seen in body length and height, caudal peduncle height and the anal fin anterior insertion point. The trophic ecomorphology of these species showed that the morpho-types that were closer to the maximum negative relative warp [(-)TR1], are associated with prey that have high speed swimming ability (Engraulidae), whereas those more similar to the maximum positive relative warp [(+)TR1] are associated with fast escape prey (crustacean). The trophic ecomorphology studied for this species, indicates that weather and availability of resources allows these individuals to use the morphological variations that they have acquired during their evolutionary history.

2009. Bohórquez-Herrera, J. Ecomorfología alimentaria de algunas especies de peces asociadas a fondos blandos. M.Sc. Thesis. Centro Interdisciplinario de Ciencias Marinas, Instituto Politécnico Nacional. La Paz, B.C.S., México. 108 p.

Reproductive aspects of three Rajiforms collected as bycatch of the shrimp trawling fishery at the Colombian Caribbean Sea.

Almost all Rajiformes are viviparous without placentas, and their embryos are nourished by yolk sacks accompanied in some cases by uterine milk. However, there are few studies of biological aspects of the species in this group in Colombia. This study aimed to analyze some reproductive aspects of Narcine bancroftii (Griffith y Smith, 1834), Diplobatis guamachensis Martin, 1957, and Rhinobatos percellens (Walbaum, 1792), captured as bycatch of the shrimp trawling fishery in two zones (north and south) of the Colombian Caribbean during the second semester of 2004. Samples were caught from the same fleet’s fishing tasks, and corresponded to one-fifth of the homogenized discard, taken randomly from  one  of  the  four  nets in the ship. 

Individuals of the three species were brought to the laboratory for further morphometry measurements, taxonomic identification and determination of the maturity state. The maturity state differentiation was based on claspers development and sperm presence for males, and in the size and development of the ovaries, eggs, and embryos for females. Females of N. bancroftii showed immaturity and spawned states, while the males were mature. The individuals of D. guamachensis were represented by maturity females with embryos, and maturity males, whereas those of R. percellens were characterized as maturity females with embryos and spawned states, and maturity males. The presence of uterine milk in individuals of N. bancroftii, and embryos in D. guamachensis were the first known reports in the literature for this country.

2007. Acevedo, K., J. Bohórquez-Herrera, C. Moreno, E. Molina, M. Grijalba-Bendeck, P. Goméz-Canchong. Reproductive aspects of three Rajiforms collected as bycatch of the shrimp trawling fishery at the Colombian Cabaribbean Sea. Annual Gulf and Caribbean Fisheries Institute. 58: 229-236. ISSN: 1553-8486.

Sharks and Rays (Subclass Elasmobranchii) discarded from commercial shrimp trawlers at the Caribbean Sea of Colombia.

In order to have an approximation to the cartilaginous fishes assemblage structure exploited by commercial shrimp trawlers from the north coast of Colombia, composition and abundance of the discarded sharks and rays on two zones of the Colombian Caribbean, between August and November of 2004 were evaluated. Eachmonth, a number of trawls were analyzed in each zone (north: La Virgen and Portete; south: Barú, Cabo Tiburón, Cascajal, Cispatá, Morrosquillo, Ceycén, Mestizo, Cedro river, Tigua and Tortuguilla). Observers were placed on board commercial shrimp trawlers, sampling 1/5 from the total capture, previously homogenized, which was randomly taken from one of the four nets of the vessel. Within 30 trawls, there were 47 cartilaginous fishes registered, belonging to six families and eight species. The largest capture per effort unit (CPUE) in biomass was registered on September in both zones, whereas the smallest happened on November in the south one. The greatest value in number of units was in September within the south zone and the opposite occurred in November, registering the smallest values. This could explain the great availability of the objective resource, directly associated with the heavier rainy season that enriches the waters of the coastal environment and characterizes the region, probably used as habitat and feeding grounds for the cartilaginous fishes.

2007. Acevedo, K., J. Bohórquez-Herrera, C. Moreno, E. Molina, M. Grijalba-Bendeck, P. Goméz-Canchong. Sharks and Rays (Subclass Elasmobranchii) discarded from commercial shrimp trawlers at the Caribbean Sea of Colombia. Acta Biológica Colombiana, 12(2): 69-80.

Biological and fishery aspects of Elasmobranchs captured in the Natural National Park Gorgona Island, and its influence area, between 2004 and 2005. (B.Sc. thesis)

Some biological and fishery aspects were analyzed in nine species of sharks (Squatina californica, Squatina sp., Heterodontus mexicanus, Mustelus spp., Carcharhinus leucas, C. limbatus, C. porosus, Rhizoprionodon longurio and Sphyrna lewini) and five of rays (Raja velezi, Zapteryx xyster, Dasyatis longa, Aetobatus narinari and Rhinoptera steindachneri) captured by espinel and calabrote in the Gorgona National Natural Park and their influence area in the 2004 and 2005 years. It wasn't find incidence of environmental factors (temperature, precipitation and salinity) in the structure of the assembly of themselves in the study area. It was obtain the bigger CPUE in number of individuals by Mustelus spp. followed by Dasyatis longa, which presented the highest values of CPUE in biomass, being this two, the only species that allow the biological analysis because of their number of individuals. 

It was registered an individual of D. longa that beat the literature sizes (3,8 m of TL and 1,8 m of WD); in the reproductive topic, the study area is principally frequent by females and it exists a bigger abundance of immature individuals than the ones who have reached their sexual maturity. Besides that, it were note a tendency of the Elasmobranchii to reproduce in the second semester of the year suggesting for Mustelus spp. a reproductive cycle of at least 10 months (June to March). It was conclude that the espinel is a selective fishery art for Mustelus spp. but not for D. longa, where the majority of the capture individuals are young than the adults. The calabrote, showed to be a fishery art much more selective and therefore, more sustainable for the long tail stingray populations. 

The food habits for both species (Mustelus spp. and D. longa), are dominated by crustacean of genera Portunus and Squilla; however, the fishes and mollusks contribute considerably to their diets also. Moreover, the two species are specialists as a mechanism to reduce the diffuse competence and increase the probability of coexistence in the area with other predators; and although both species share some prey categories, they don't present a significant overlap diet.

2006. Bohórquez-Herrera, J. Aspectos biológicos y pesqueros de elasmobranquios capturados en el Parque Nacional Natural Gorgona y su área de influencia entre 2004 y 2005. B.Sc. Thesis: Marine Biologist. Universidad Jorge Tadeo Lozano. Bogotá, Colombia. 105 p.

Characterization and some biological aspects of the sharks and rays  assembly (Subclass Elasmobranchii) discarded by the shrimp trawling fishery in the Colombian Caribbean between August and November of 2004. (B.Sc. seminar - academic exercise)

  • Las especies encontradas son en su mayoría bentónicas a excepción de Sphyrna tiburo y Rhizoprionodon porosus que presentan hábitos demersales, esta característica hace que N. bancroftii, D. guttata, R. percellens, D. guamachensis y U. jamaicensis sean susceptibles de ser capturadas en los arrastres camaroneros.
  • La captura por unidad de esfuerzo es mayor para el mes de septiembre en las dos zonas, pero difieren en el número total de individuos que es mayor en la zona sur.
  • La zona sur en el sector de golfo de Morrosquillo presentó una mayor abundancia de especies capturadas, lo cual puede atribuirse a que es un área donde se realizan con mayor intensidad las faenas de pesca de camarón, lo cual puede estar asociado a la gran variedad de complejos lagunares originados por el antiguo delta del río Sinú que enriquece la zona.
  • La presencia de individuos en la zona norte puede explicarse por la cercanía de bahía Portete, la cual posee variedad de ecosistemas con características apropiadas para el desarrollo de las especies.
  • El mes que registró el mayor número de individuos y especies fue septiembre, debido posiblemente a la influencia de la época lluviosa.
  • Un factor determinante es la estructura del ensamblaje de elasmobranquios asociados a la pesca camaronera, puede ser la cercanía de ecosistemas como pastos marinos, estuarios y manglares.
  • Las especies Narcine bancroftii, Rhinobatos percellens y Dasyatis guttatase registraron para ambas zonas, por lo cual ratifica su amplio rango de distribución en el Caribe colombiano, haciéndolas susceptibles de ser capturadas por el arrastre camaronero.
  • Se confirma la presencia de la leche uterina en las hembras grávidas de Narcine bancroftii, la cual se encuentra esparcida rodeando a los embriones y se corrobora la condición ovovivípara de Rhinobatos percellens, por la presencia de un recubrimiento que aislaba a los embriones dentro del ovario de la madre. 
  • Rhinobatos percellens y Diplobatis guamachensis, posiblemente muestren ciclos reproductivos asincrónicos ya que presentan crías con diferencias en tamaño y número en la misma camada, los embriones de ambas especies presentan el mismo patrón de coloración de los adultos.

2005. Acevedo, K., J. Bohórquez-Herrera, C. Moreno, F. Moreno, E. Molina. Caracterización y algunos aspectos biológicos del ensamblaje de tiburones y rayas (Subclase Elasmobranchii) descartado por la flota camaronera en el Caribe colombiano entre agosto y noviembre del 2004. Research Seminar, Faculty of Marine Biology. Universidad Jorge Tadeo Lozano, Santa Marta, Colombia. 90 p.

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