ecología-junio2024

Perfil de leucocitos como biomarcador hematológicoen poblaciones de la salamandra de arroyo Ambystoma ordinarium

Carolina González-Pardo ^a, Ireri Suazo-Ortuño ^a,*, Cinthya Mendoza-Almeralla ^b, David Tafolla-Venegas ^c, Yurixhi Maldonado-López ^a y Esperanza Meléndez-Herrera ^a

^aUniversidad Michoacana de San Nicolás de Hidalgo, Instituto de Investigaciones sobre los Recursos Naturales, Avenida San Juanito Itzícuaro s/n, Nueva Esperanza, 58330 Morelia, Michoacán, México

^bUniversidad Autonóma del Estado de Hidalgo, Instituto de Ciencias Básicas e Ingeniería, Centro de Investigaciones Biológicas, Laboratorio de Ecología de Poblaciones, Km 4.5 carretera Pachuca-Tulancingo, 42184 Mineral de La Reforma, Hidalgo, México

^cUniversidad Michoacana de San Nicolás de Hidalgo, Facultad de Biología, Edificio R, Ciudad Universitaria, 58030 Morelia, Michoacán, México

*Autor de correspondencia: ireri.suazo@umich.mx (I. Suazo-Ortuño)

Recibido: 7 agosto 2023; aceptado: 22 febrero 2024

Resumen

La evaluación del perfil de leucocitos como biomarcador hematológico en las poblaciones de anfibios es cada vez más común en estudios ecológicos en especies amenazadas o en declive. En este estudio evaluamos y comparamos el perfil de leucocitos y el índice neutrófilos/linfocitos (N/L) en frotis de sangre periférica de Ambystoma ordinarium en 3 tipos de hábitats: conservados, urbanizados y agrícolas. Consideramos al perfil leucocitario como un endpoint inmunológico, ya que nos puede proporcionar información sobre la respuesta inmunológica del organismo. De acuerdo con los resultados encontrados, en los individuos de A. ordinarium de los sitios urbanizados y agrícolas se detectaron aumentos en las proporciones de eosinófilos, basófilos y monocitos, y una disminución en las proporciones de linfocitos. Asimismo, en los individuos de los sitios urbanizados y agrícolas se detectaron aumentos en el número de neutrófilos banda, además se reporta por primera vez el hallazgo de células plasmáticas en la sangre de esta especie. En general, los perfiles de leucocitos de los individuos de A. ordinarium en los sitios urbanizados y agrícolas observados en este estudio, podrían interpretarse como respuestas fisiológicas a la perturbación ambiental.

Palabras clave: Hábitats perturbados; Respuesta inmunitaria; Índice N/L; Neutrófilos banda; Células plasmáticas; Achoque michoacano

(http://creativecommons.org/licenses/by-nc-nd/4.0/).

Leukocyte profile as hematologic biomarker in populations of the mountain salamander, Ambystoma ordinarium

Abstract

Assessing the leukocyte profile as a hematological biomarker is now frequently used in ecological studies of threatened or declining species. In this study, we evaluated and compared leukocytes profile and neutrophils/lymphocytes (N/L) ratio in peripheral blood smears of the salamander Ambystoma ordinarium in 3 types of habitats: urbanized, agricultural, and conserved. We considered leukocyte profiles as an immunological endpoint, since it can provide information about the immunological response. Results indicated that A. ordinarium individuals from the urbanized and agricultural sites presented higher proportions of neutrophils, eosinophils, basophils and monocytes and a decrease in the proportions of lymphocytes. Agricultural habitats presented higher N/L ratios. Likewise, in the individuals of urbanized and agricultural sites an increase was registered in the number of neutrophils with a band nucleus, in addition, the finding of plasma cells in the blood of this species is reported for the first time. In general, leukocyte profiles of A. ordinarium individuals in urbanized and agricultural sites observed in this study suggest that these profiles can be interpreted as physiological responses to environmental disturbance.

Keywords: Disturbed habitats; Immune response; N/L ratio; Band neutrophils; Plasma cells; Achoque michoacano

Introducción

En la actualidad, una de las preocupaciones más importantes en la conservación de vida silvestre es la pérdida y disminución global de las especies de anfibios (Alvarado, 2021). Los cambios en los hábitats asociados a las actividades antropogénicas y las enfermedades infecciosas representan las principales amenazas (Wake y Vredenburg, 2008). Sin embargo, científicos en todo el mundo, consideran que no existe una sola causa potencial, sino que éstos y otros factores pueden actuar mediante sinergias contribuyendo en la disminución de sus poblaciones (Lips et al., 2005; Stuart et al., 2004).

Los anfibios, pueden ser más vulnerables a los cambios en sus hábitats en comparación con el resto de los vertebrados, por 2 razones principales: poseen una piel delgada y porosa que es permeable al agua, y son organismos ectotermos, por lo que dependen de su entorno para conservar su temperatura (Duellman y Trueb, 1994). Por estos motivos, la evaluación del estado de salud de las poblaciones de anfibios es cada vez más común en estudios ecológicos en especies amenazadas o en declive (Barriga-Vallejo et al., 2015; Das y Mahapatra, 2014; Shutler y Marcogliese, 2011). Los perfiles de leucocitos han sido evaluados con mayor frecuencia porque proporcionan información sobre el estado inmunológico y permiten detectar cambios fisiológicos y patológicos tempranos en los individuos, sobretodo, estudios recientes han comenzado a incorporarlos como biomarcadores para evaluar la salud de los individuos y de su ambiente (Barni et al., 2007; Cabagna et al., 2005; Davis et al., 2010; Salinas et al., 2015, 2019).

Los leucocitos (linfocitos, neutrófilos, eosinófilos, basófilos y monocitos) son células sanguíneas que forman parte del sistema inmunitario, desempeñando funciones cruciales en la defensa contra infecciones y enfermedades (Thrall, 2004). De esta forma, los leucocitos en sangre pueden aumentar rápidamente en una infección, por ejemplo, aumentos en las proporciones de eosinófilos se han asociado con infecciones parasitarias (Davis y Golladay, 2019; Ramírez-Hernández et al., 2019) y en evidencia reciente, se han reportado aumentos en las frecuencias de linfocitos maduros e inmaduros (Salinas et al., 2019). El perfil de leucocitos también ha sido evaluado con éxito como indicador de estrés en poblaciones en ambientes perturbados y alteraciones morfológicas como el aumento de neutrófilos sin segmentación nuclear se han relacionado con ambientes contaminados con desechos urbanos y agrícolas (Barni et al., 2007; Cabagna et al., 2005; Ramírez-Hernández et al., 2019; Romanova y Romanova, 2003).

En México, habitan 14 especies del género Ambystoma (Ramírez-Bautista et al., 2023) y se ha estudiado el perfil de leucocitos en algunas especies como biomarcador de inflamación y estrés asociado a perturbaciones antropogénicas (Barriga-Vallejo et al., 2015; Ramírez-Hernández et al., 2019). La salamandra de arroyo Ambystoma ordinarium se distribuye en el noreste de Michoacán y se encuentra catalogada como en peligro de extinción por la IUCN (2024), y como especie protegida por el gobierno de México (Semarnat, 2010). Particularmente, en varios sitios del área de distribución de esta especie existe un fuerte impacto sobre los arroyos que habita debido a presiones de urbanización, actividades agrícolas y ganaderas (Soto-Rojas, 2012). Considerando el contexto en el que se encuentra esta especie, es importante monitorear sus poblaciones, sobre todo las que están sujetas a la continua perturbación de sus hábitats. Por lo tanto, el objetivo de este estudio fue evaluar y comparar los perfiles de leucocitos como biomarcador hematológico en poblaciones de A. ordinarium de hábitats con diferentes grados de perturbación: conservados, urbanizados y agrícolas.

Materiales y métodos

Se realizaron 2 visitas, la primera en noviembre de 2020 y la segunda en marzo de 2021 a 9 sitios con arroyos habitados por A. ordinarium condiferentes grados de perturbación en Michoacán (fig. 1).Los sitios 1, 2 y 3 se encuentran en zonas conservadas en los municipios de Charo, Morelia y Zinápecuaro. En estos sitios, la vegetación está representada por bosque de pino y pino-encino y no se encuentran afectados por la urbanización, cultivos ni zonas de pastoreo.

Los sitios 4, 5 y 6 son urbanizados y se localizan en la Ciudad de Morelia, la cual tiene una extensión de 1,333 km² y presenta más de 500,000 habitantes (Magaña-Martínez y Reyes Camacho, 2012; tabla 1, fig. 1). Cada sitio se encuentra a una distancia mínima de 3 km uno con respecto a otro, por lo que corresponden a 3 poblaciones independientes de acuerdo a la poca vagilidad de la especie reportada por Montes-Calderón et al. (2011). Se consideraron los sitios como perturbados debido a: 1) la presencia de construcciones urbanas (López- Granados et al., 2008; Magaña-Martínez y Reyes Camacho, 2012), 2) el vertimiento de aguas contaminadas con fertilizantes y pesticidas (López- Granados et al., 2008) y 3) se encuentran a menos de 1 km de avenidas principales de la ciudad de Morelia (Téllez-Ramírez, 2012).

Los sitios 7, 8 y 9 se encuentran en zonas agrícolas en los municipios de Queréndaro, Indaparapeo y Zinapécuaro (fig. 1). Estos sitios presentan arroyos permanentes con escasa vegetación ribereña y se consideran perturbados porque durante el muestreo de este estudio, estaban rodeados de cultivos de maíz y potreros, y no presentaban vegetación de bosque de pino y pino-encino.

En cada arroyo se realizó una búsqueda intensiva de los ejemplares mediante la técnica de inspección por encuentro visual (VES) (Crump y Scott, 1994). Una vez localizados, se capturaron con red de mano y se colocaron en recipientes con agua de su medio para evitar su desecación. Inmediatamente, en el sitio de colecta, se manipuló a cada ejemplar con guantes estériles y se obtuvo una gota de sangre periférica de un pequeño corte de una de las branquias, llevando a cabo el procedimiento sin sacrificar a los individuos. La gota de sangre se colocó en el extremo de un portaobjetos limpio y con ayuda de un segundo, el cual se colocó en un ángulo de 45° por delante de la gota, se lo hizo retroceder hasta tocar la gota, luego se deslizó ejerciendo una presión suave y firme hacia delante. Cada frotis sanguíneo se secó a temperatura ambiente por 3 min y se fijó con metanol. Al final del procedimiento todos los organismos se liberaron en sus respectivos arroyos de origen. El manejo de las salamandras y las muestras se realizó con el permiso de colecta científica número SGPA/DGVS/13339/19 otorgado por la Semarnat.

Los frotis sanguíneos fueron llevados al laboratorio de Parasitología de la Universidad Michoacana de San Nicolás de Hidalgo (UMSNH) y se cubrieron con el colorante no diluido de Wright, dejándose reposar durante 5 min. Posteriormente, se les agregó solución buffer de Wright gota a gota, hasta que apareció una película metálica sobre la muestra, después se dejaron reposar por 5 min. Finalmente, los frotis fueron lavados con agua destilada, hasta que el colorante se lavó y se dejaron secar.

Figura 1. Mapa de la ubicación de los sitios de estudio de A. ordinarium en algunos municipios de Michoacán. 1. 5.7 km al este de Jaripeo, 2. Agua Zarca, 3. 8.9 km al oeste de Bocaneo, 4. Puente campestre, 5. Filtros viejos, 6. Río Chiquito, 7. 14 km al sur de Queréndaro, 8. 0.75 km al sur de Ziróndaro, 9. 10.86 km al sureste del Municipio de Queréndaro.

Tabla 1

Datos de colecta de Ambystoma ordinarium. Se muestra el nombre, las coordenadas y la categoría de los sitios de colecta y el número y talla de los organismos colectados.

Número y nombre de sitio	Coordenadas	Categoría del sitio	Individuos colectados en invierno 2020	Individuos colectados en primavera 2021	Longitud LHC en mm
1. 5.7 km al este de Jaripeo	19°40’28.3” N, 101°01’44.9” O	Conservado	4	3	74 a 77
2. Agua Zarca	19°34’28.9” N, 101°07’28.2” O	Conservado	3	13	66 a 77
3. 8.9 km al oeste de Bocaneo	19°50’28.6” N, 100°43’55.1” O	Conservado	0	13	67 a 88
4. Puente campestre	19°40’31.3” N, 101°09’27.5′′ O	Urbanizado	3	3	79 a 98
5. Filtros Viejos	19°40’01.0” N, 101°08’36” O	Urbanizado	5	8	77 a 91
6. Río Chiquito	19°36’38.2” N, 101°07’26.8” O	Urbanizado	7	5	81 a 101
7. 14 km al sur de Queréndaro	19°41’05.2” N, 100°52’31.2” O	Agricola	5	11	75 a 94
8. 0.75 km al sur de Ziróndaro	19°42’58.4” N, 100°54’59.6” O	Agricola	9	8	67 a 118
9. 10.86 km al sureste del Municipio de Queréndaro	19°45’25.4” N, 100°50’33.9” O	Agricola	4	5	82 a 111

Cada frotis se observó al microscopio óptico con el aumento 400x y se efectuó el recuento diferencial de leucocitos en movimiento zigzag. Las células fueron contadas por una sola persona para evitar la variabilidad en las observaciones considerando las características morfológicas descritas por Thrall (2004), Hadji-Azimi et al. (1987) y Salinas et al. (2017). Siguiendo a Davis et al. (2008), en cada frotis sanguíneo se contaron 100 células, determinándose las proporciones relativas de los 5 tipos de leucocitos y el índice N/L propuesto como indicador de respuesta al estrés. Para la evaluación morfológica de los leucocitos, durante el recuento diferencial, se contaron los leucocitos con cambios en la coloración y presencia de manifestaciones morfológicas en el citoplasma; además, se evaluó la segmentación nuclear de los neutrófilos (neutrófilos banda, identificados por la falta de segmentación en el núcleo).

Para comparar las proporciones y la morfología de cada tipo de leucocito y los índices N/L de los individuos de A. ordinarium entre los sitios conservados, urbanizados y agrícolas, se utilizaron modelos lineales generalizados mixtos (GLM), con error de distribución Poisson debido a que las variables de respuesta son conteos. Los análisis estadísticos se realizaron en R versión 4.2.0 (R Core Team, 2022) y se usó el paquete ggplot2 versión 3.4.1 (Wickham et al., 2016) para la realización de figuras.

Resultados

Se recolectaron 109 individuos de Ambystoma ordinarium en los 3 sitios, 36 en conservados, 31 en urbanizados y 42 en los agrícolas (tabla 1), 40 ejemplares se obtuvieron en invierno de 2020 y 69 en primavera de 2021. El promedio de la longitud total de los ejemplares fue de 82.44 mm (mínima 66-118 máxima) y de acuerdo con las tallas reportadas por Anderson y Worthington (1971), todos los individuos recolectados fueron adultos metamórficos (tabla 1).

Los promedios en las proporciones de los 5 tipos de leucocitos y el índice N/L de los individuos de A. ordinarium para los sitios conservados, urbanizados y agrícolas se presentan en la tabla 2. Las proporciones de linfocitos mostraron diferencias significativas entre los sitios. Se detectaron disminuciones en las proporciones de estas células en individuos de los sitios urbanizados y agrícolas en comparación con los individuos de los hábitats conservados (fig. 2). No se detectaron diferencias en las proporciones de neutrófilos y los índices N/L entre los sitios (tabla 2). Por último, las proporciones de eosinófilos, basófilos y monocitos mostraron diferencias significativas entre los sitios (tabla 2). Se detectaron aumentos en las proporciones de estas células en individuos de los sitios urbanizados y agrícolas con respecto a los individuos de los sitios conservados (fig. 2).

Figura 2. Gráfica de cajas y alambres que muestra las diferencias en las proporciones de leucocitos entre los hábitats urbanizados, agrícolas y conservados. Las letras representan las diferencias de medias entre grupos de acuerdo al GLM.

Los linfocitos, fueron los leucocitos de menor tamaño, la mayoría de éstos se caracterizaron por ser células redondas con un núcleo central que ocupó la mayor parte del citoplasma basófilo (fig. 3). En los frotis sanguíneos de 2 individuos de los hábitas agrícolas se observaron células plasmáticas, caracterizadas por un núcleo excéntrico, citoplasma abundante con aumento en la basofília y abundantes inclusiones globulares y hialinas (fig. 3).

Tabla 2

Promedios relativos de los leucocitos e índices N/L (±error estándar) en individuos adultos de Ambystoma ordinarium entre hábitats conservados, urbanizados y agrícolas.

Variable de respuesta	Hábitats conservados	Hábitats urbanizados	Hábitats agrícolas	gl	c²	p
Linfocitos	83.1 (± 0.51)	72.8 (± 1.20)	74.5 (± 0.93)	2	27.84	< 0.001
Neutrófilos	8.4 (± 0.69)	8.9 (± 0.95)	9.6 (± 0.97)	2	2.84	0.095
Eosinófilos	3.9 (± 0.38)	8.3 (± 1.53)	9.0 (± 0.84)	2	88.37	< 0.001
Basófilos	2.7 (± 0.42)	4.9 (± 0.68)	4.5 (± 0.52)	2	26.66	< 0.001
Monocitos	1.7 (± 0.43)	4.9 (± 1.24)	2.2 (± 0.39)	2	63.26	< 0.001
Neutrófilos banda	1.5 (± 0.24)	3.1 (± 0.60)	3.8 (± 0.48)	2	42.27	<0.001
Índice N/L	0.10 (± 0.00)	0.10 (± 0.011)	0.13 (± 0.01)	2	0.17	0.698

Los neutrófilos se caracterizaron por ser células redondas irregulares que pueden o no presentar finos gránulos en el citoplasma, su núcleo violeta puede no presentar segmentaciones (neutrófilos banda, fig. 3) ó ser segmentados de 2 a 5 lóbulos (fig. 3). En relación con la comparación de la segmentación nuclear de los neutrófilos entre los sitios, se encontraron variaciones significativas, detectándose incrementos en las proporciones de neutrófilos banda en individuos de los sitios urbanizados y agrícolas con respecto a los individuos de los sitios conservados (fig. 3).

Los eosinófilos fueron células con abundantes gránulos rosados cubriendo el citoplasma, presentan un núcleo violeta generalmente bilobulado (fig. 3) y en pocas ocasiones se observó unilobulado y trilobulado. Con respecto de la morfología de los basófilos, éstos se caracterizaron por ser células redondas u ovaladas con abundantes gránulos púrpuras en el citoplasma que, por lo general, cubren el núcleo redondo o bilobulado (fig. 3). Por último, los monocitos fueron los leucocitos de mayor tamaño, son células redondas con núcleo en forma de riñón o herradura y citoplasma abundante (fig. 3). No se observaron variaciones morfológicas en eosinófilos, basófilos y monocitos.

Discusión

Se evaluaron los perfiles de leucocitos en frotis de sangre de 109 individuos adultos de la salamandra Ambystoma ordinarium, de los cuales 37 se recolectaron en hábitats conservados, 30 en hábitats urbanizados y 42 en hábitats agrícolas. La morfología y coloración de los 5 tipos de leucocitos concuerdan con lo reportado para otras especies de anuros y caudados (Cabagna et al., 2005; Hadji-Azimi et al., 1987; Salinas et al., 2017). Los linfocitos fueron los leucocitos más abundantes, detectándose disminuciones en sus proporciones en individuos de A. ordinarium de los sitios urbanizados y agrícolas considerados como perturbados. En estudios recientes, la disminución de los linfocitos en sangre se ha documentado en especies de anfibios como respuesta a factores estresantes como infecciones y hábitats contaminados con pesticidas, debido a que el aumento en las hormonas del estrés (glucocorticoides) puede inducir la salida de estas células de la sangre a los tejidos linfoides (en anfibios, hígado y bazo) (Davis et al., 2008; Waye et al., 2019). En contraste, los neutrófilos por ser las principales células encargadas del ataque a agentes infecciosos son estimulados a proliferar para migrar a los sitios de inflamación. La disminución en las proporciones de los linfocitos se ha relacionado con el aumento en las proporciones de los neutrófilos (índice N/L) como biomarcador de estrés (Davis et al., 2010). En este estudio, no se detectaron variaciones significativas en las proporciones de neutrófilos y en los índices N/L promedio. En estudios previos en poblaciones silvestres de salamandras del género Ambystoma y otras especies de anfibios, se han reportado índices N/L promedio cercanos a 0.40 (Cabagna et al., 2005; Davis y Durso, 2009; Shutler et al., 2009). Sin embargo, a diferencia de nuestro estudio, Ramírez-Hernández et al. (2019) reportaron para esta especie un índice N/L promedio de 1.5. y 0.9 en hábitats perturbados y conservados, respectivamente. Las diferencias entre ambos resultados podrían deberse a que el tamaño de muestra utilizado por Ramírez-Hernández et al. (2019) fue pequeño en comparación con el tamaño de muestra utilizado en nuestro estudio. Además, nuestros resultados pueden indicar que otros factores no contabilizados están influyendo en las respuestas de estas células en los individuos muestreados. Un factor que aumenta el índice linfocitos y neutrófilos en anfibios es la infección por Batrachochytrium dendrobatidis (Bd; Davis et al., 2010; Savage et al., 2016). Recientemente, se reportó la presencia del hongo quitridio en las mismas poblaciones de A. ordinarium analizadas en este estudio (Mendoza-Almeralla et al., 2023). Los niveles de infección por Bd reportados fueron de entre 112 a 1,856 equivalentes zoosporas genómicas (EZG´s) en 2 sitios conservados; mientras que en los sitios perturbados, el grado de infección fue de 21 a 4,338 EZG´s, ésto sugiere que hay mayor grado de infección en lugares perturbados. Por lo que es importante saber si el número de neutrófilos y linfocitos es afectado por la infección del quitridio.

Figura 3. Leucocitos en frotis de sangre periférica de A. ordinarium. A) Linfocito, B) neutrófilo segmentado, C) neutrófilo banda, D) eosinófilo, E) basófilo, D) monocito, vista a 100X, G) célula plasmática con núcleo excéntrico y citoplasma abundante, vista a 40X.

Por otro lado, se detectaron incrementos de neutrófilos banda en individuos de los sitios perturbados con respecto a los sitios conservados. En procesos inflamatorios, los neutrófilos son impulsados a proliferar y para compensar esta demanda, la médula ósea libera en la sangre células inmaduras (neutrófilos banda) (Davis y Golladay, 2019). En anfibios existe evidencia de incrementos en las proporciones de estas células como respuesta inflamatoria contra fertilizantes y pesticidas (Mann et al., 2009; Romanova et al., 2022). Pese a que en este estudio no evaluamos la presencia de estos contaminantes químicos en el agua, en los sitios urbanizados seleccionados aquí, se han reportado descargas de aguas contaminadas con fertilizantes y pesticidas (López-Granados et al., 2008), y en los sitios agrícolas es probable que el uso de estos agroquímicos sea habitual y su dispersión fuera de estas áreas pueda llegar hasta los arroyos donde habita esta especie. Los incrementos detectados en las proporciones de eosinófilos, basófilos y monocitos en los individuos de los sitios urbanizados y agrícolas también se pueden asociar con la presencia de estos contaminantes químicos en sus hábitats. En algunos estudios en anfibios se han reportado incrementos en las proporciones de eosinófilos en sitios contaminados por pesticidas por su capacidad de reaccionar a antígenos ambientales (Attademo et al., 2014; Romanova y Romanova, 2003). Con respecto a los monocitos, el aumento de estas células podría relacionarse con el incremento de la fagocitosis de desechos tisulares, puesto que, de acuerdo con algunos autores la exposición prolongada a contaminantes químicos aumenta la necrosis tisular (Zhelev, 2007). El papel de los basófilos en las respuestas inmunitarias de los anfibios no es claro (Allender y Fry, 2008), sin embargo, al igual que en otros grupos de vertebrados parecen desempeñar un papel importante en la inflamación (Claver y Quaglia, 2009).

Los estudios realizados por varios investigadores han revelado que los anfibios son capaces de generar una respuesta inmunitaria a antígenos complejos asociados con patógenos y antígenos ambientales (Grogan et al., 2018; Savage y Zamudio, 2011; Zhelev, 2007). Los linfocitos (células T y B), ante la presencia de antígenos son responsables de activar la inmunidad mediada por células específicas de patógenos (células T citotóxicas o auxiliares) y la inmunidad humoral (células plasmáticas secretoras de anticuerpos específicos) (Grogan et al., 2018). El hallazgo de células plasmáticas en la sangre de los individuos de los sitios agrícolas podría atribuirse a la especificidad de la respuesta inmune humoral a antígenos tóxicos presentes en el ambiente. En un estudio previo, Zhelev (2007) reportó aumentos de estas células en individuos de Rana ridibunda en hábitats con contaminación industrial. El hallazgo de estas células es interesante, porque casi no hay datos en la literatura sobre su presencia y apariencia en la sangre de los anfibios. Aunque no podemos asegurar que se trate de este tipo de células, estos datos sin duda sientan las bases para desarrollar estudios bioquímicos e inmunológicos futuros.

En anfibios se ha documentado la función antipara-
sitaria de los eosinófilos en infecciones con nemátodos y tremátodos (Belden y Kiesecker, 2005; Davis y Golladay, 2019; Kiesecker, 2002; Rohr et al., 2008). Particularmente, Ramírez-Hernández et al. (2019) reportaron aumentos en las cargas parasitarias en poblaciones de A. ordinarium por 2 especies de tremátodos, Gorgoderina attenuata y Ochetosoma sp.,y 2 especies de nemátodos Cosmocercoides sp.y Hedruris siredonis en hábitats perturbados, siendo uno de estos hábitats correspondiente al sitio Río Chiquito de este estudio. Adicionalmente, Mendoza-Almeralla et al. (2023) reportaron la infección por el nemátodo del género Capillaria en el sitio Filtros viejos. Por lo tanto, los incrementos de eosinófilos detectados en los individuos de estos sitios, podrían relacionarse con la presencia de mayor prevalencia de infecciones parásitarias.

Finalmente, los perfiles de leucocitos de los individuos de A. ordinarium en este estudio proporcionan parámetros hematológicos de comparación entre distintas poblaciones. De acuerdo con nuestros resultados, la evaluación de los perfiles de leucocitos es uno de los métodos más simples y menos invasivos. Los cambios en sus valores, especialmente en las poblaciones de hábitats perturbados, pueden utilizarse con éxito en evaluaciones futuras para detectar cambios fisiológicos y patológicos tempranos en los individuos y puede ser una señal de advertencia de degradación ambiental. Sin embargo, es importante reiterar que interpretar las proporciones de los leucocitos puede ser complicado, debido a que los leucocitos pueden responder a diversos factores (Barni et al., 2007; Cabagna et al., 2005; Romanova y Romanova, 2003; Shutler y Marcogliese, 2011; Shutler et al., 2009). Por ello es necesario llevar a cabo estudios complementarios sobre enfermedades infecciosas, calidad del agua, niveles de hormonas de estrés, presencia de pesticidas o metales pesados, entre otros, que permitan relacionar y estudiar la respuesta de los leucocitos en las poblaciones de esta especie y otras especies de anfibios con los diversos factores o contextos en los que se encuentran estas especies.

Agradecimientos

Este estudio fue parte del proyecto “Descifrando el microbioma de la piel en ajolotes y las consecuencias de la interacción huésped microbioma sobre una enfermedad letal emergente” de la Secretaría de Educación Pública/Consejo Nacional de Humanidades, Ciencias y Tecnologías Ciencias de Frontera. FORDECYT-PRONACES/373914/2020. Los resultados de este estudio forman parte de la tesis de maestría del autor principal, bajo la dirección de ISO y CMA. CGP agradece el apoyo financiero del Programa Nacional de Becas de SEP/Conahcyt.

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Ephemeral and intermittent xeroriparian systems arekeystone habitats for bird communities during thenon-breeding season in a Mexican semiarid landscape

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Mónica E. Riojas-López ^a, Eric Mellink ^b,*, Moisés Montes-Olivares ^b

^a Universidad de Guadalajara, Centro Universitario de Ciencias Biológicas y Agropecuarias, Departamento de Ecología, C. Ramón Padilla Sánchez Núm. 2100, 45100 Zapopan, Jalisco, Mexico

^b Centro de Investigación Científica y de Educación Superior de Ensenada, Departamento de Biología de la Conservación, Carretera Ensenada-Tijuana Núm. 3918, Zona Playitas, 22860 Ensenada, Baja California, Mexico

*Corresponding author: emellink@cicese.mx (E. Mellink)

Received: 23 October 2023; accepted: 9 April 2024

Abstract

Intermittent and ephemeral xeroriparian systems cover less than 1% of continental North America and are critical for wildlife in arid and semi-arid areas but are understudied and absent from conservation plans. We report the diversity of birds in 3 xeroriparian systems of the Mexican Altiplano during the non-breeding season and the habitat variables that influence them. Of the 48 documented species in this study, we have recorded 15 only in these systems, throughout our long-time research in the region. Bird communities were positively influenced by minimum and maximum height of shrubs and trees and negatively by canopy cover. The communities were grouped in one gradient from lower richness in rocky, entrenched streams, with closed canopy and little herbaceous vegetation, to greater richness in wide, open streams, with abundant herbaceous plants, and in a second gradient, from insectivorous to granivorous birds. Our study covered habitats not considered in other similar studies in Mexico and revealed that at the landscape level, ephemeral and intermittent xeroriparian systems could play a crucial role in conservation given that the systems studied covered approximately 0.1% of the area but hosted 20% of the region’s land bird species and, among migrants, especially Spring migrants.

Keywords: Arid lands; Semiarid lands; Llanos de Ojuelos; Anthropized landscapes; Migratory birds

(http://creativecommons.org/licenses/by-nc-nd/4.0/).

Los sistemas xeroribereños efímeros e intermitentes son hábitats clave para comunidades de aves en la temporada no reproductiva en un paisaje semiárido mexicano

Resumen

Los hábitats xeroribereños intermitentes y efímeros cubren menos de 1% de la superficie continental de Norteamérica y son críticos para la fauna silvestre de zonas áridas y semiáridas, pero están poco estudiados y ausentes de planes de conservación. Reportamos la diversidad de aves en 3 sistemas xeroribereños del Altiplano Mexicano durante la temporada no reproductiva y las variables del hábitat que influyen. De 48 especies documentadas, hemos registrado 15 solo en sistemas xiroribereños en muchos años de investigación en la región. Arbustos y árboles más altos tuvieron influencia positiva en la comunidad de aves, mientras que doseles cerrados la tuvieron negativamente. Las comunidades se agruparon de menor riqueza en arroyos rocosos y encañonados con dosel cerrado y poca vegetación herbácea, a mayor riqueza en arroyos amplios y abiertos con abundantes herbáceas, y en un segundo gradiente, de aves insectívoras a granívoras. Nuestro estudio cubrió hábitats no considerados en otros trabajos similares en México y reveló que a nivel de paisaje, los sistemas xeroribereños efímeros e intermitentes podrían ser importantes en la conservación: los sistemas estudiados cubrían aproximadamente 0.1% del área, pero albergaron 20% de las especies de aves terrestres de la región, y entre especies migrantes, especialmente las de primavera.

Palabras clave: Zonas áridas; Zonas semiáridas; Llanos de Ojuelos; Paisajes antropizados; Aves migratorias

Introduction

Riparian systems are plant communities that develop as a result of perennial, intermittent, or ephemeral surface or subsurface water (Krueper, 1993). These systems are one of the rarest habitats in North America and cover less than 5% of the continental land mass (Krueper, 2000). Despite their rarity, throughout the world, riparian systems are extremely important because of their disproportionate contribution, relative to area, for biodiversity conservation (Arizmendi et al., 2008; Carlisle et al., 2009; Hinojosa-Huerta et al., 2013; Kirkpatrick et al., 2009; Knopf, 1985; Krueper 1993, 1996, 2000; Seymour & Simmons, 2008; Skagen et al., 1998; Wilson in Knopf et al., 1988). They also contribute to enhance connectivity in fragmented landscapes particularly for resident and non-migrating birds (Şekercioǧlu et al., 2015).

Dryland riparian systems are known as xeroriparian, and whether the streams that originate them are perennial, or non-perennial, they are notoriously different from the surrounding landscape. In the western United States, in the 1980s they covered < 1% of the land (Knopf et al., 1988). However, they are very important for wildlife in semiarid and arid regions, and support much of the biotic diversity in semiarid and arid southwestern USA (Sánchez-Montoya et al., 2017; Szaro & Jakle, 1985), sometimes having bird population densities and species diversity as much as 5 to 10 times those of nearby desert non-riparian systems (Johnson & Haight, 1985; Levick et al., 2008). In these regions, migrating birds depend on water, habitat, and food that are restricted spatially and temporally (Carlisle et al., 2009). Up to 70% of all bird species use riparian systems in drylands at some point in their life cycle (Krueper, 1996), and > 60% of the neotropical migratory bird species use them either as stopover areas or as breeding habitats (Kirkpatrick et al., 2009; Krueper, 1993; Skagen et al., 1998).

Although non-perennial streams are the most widespread flowing-water ecosystem throughout the world (Datry et al., 2017), ecological studies on xeroriparian systems had focused mostly on permanent streams (Hinojosa-Huerta et al., 2013; Neate-Clegg et al., 2021; Szaro & Jakle, 1985). Overall, riparian systems created and maintained by intermittent and ephemeral streams are understudied and the scientific literature on their ecological role is very limited (Datry et al., 2017; Levick et al., 2008; McDonough et al., 2011; Sánchez-Montoya et al., 2017). Not only are they understudied, but they also are poorly considered in conservation planning. For example, intermittent and ephemeral streams are recognized in California´s “Riparian Bird Conservation Plan” (Riparian Habitat Joint Venture, 2004), but only perennial ones are included in its actions. Such neglect of largely intermittent or ephemeral riparian systems can lead to serious shortcomings in conserving biodiversity.

Xeroriparian systems are important not only for biodiversity, but the water in them has been a coveted commodity for human survival and productive activities, and, in consequence, they have suffered extreme, widespread modification. As a result, within the past 100 years an estimated 95% of lowland riparian habitat in western North America has been altered, degraded, or destroyed (Krueper, 2000). In arid and semiarid regions where water is naturally scarce, livestock and agricultural demands for it result in riparian systems being affected with particular severity (Patten et al., 2018). Mexico´s arid and semiarid Central Altiplano is no exception, and its riparian systems have been transformed by their water being diverted for human needs with no consideration for the conservation of wildlife (Mellink & Riojas-López, 2005).

Published information on non-urban xeroriparian systems is scarce, and for Mexico, it is even scarcer. The only 3 articles in the scientific literature that we have found on birds in xeroriparian systems in Mexico focus on perennial systems (Arizmendi et al., 2008; Hinojosa-Huerta et al., 2013; Pérez-Amezola et al., 2020). Three highly relevant nationwide biodiversity conservation sources surprisingly do not mention riparian systems: 1) A 1998 listing of Mexico´s natural protected areas (Conabio, 1998); 2) the extensive treatise on the use and conservation of the terrestrial ecosystems of Mexico (Challenger, 1998); and 3) the 3 volume, 1,739 pages, Estado de Mexico´s biodiversity and its conservation threats (Conabio, 2008). This suggests that in addition to being understudied, the importance of riparian systems in Mexico has not been fully appreciated.

One of the least studied landscape components of the southern Mexican Altiplano, including the Llanos de Ojuelos, are xeroriparian systems. This region is strongly anthropized and natural habitats have been greatly affected by agriculture and livestock, including the riparian systems in it. Currently, those riparian systems in the region that have not disappeared because of water channelization and damming, are subject to browsing and trampling by livestock, and by the extraction of wood, sand, gravel, and water. However, the remaining xeroriparian systems in the southern part of this Altiplano, even in their impacted form, continue to provide habitat for wildlife (Riojas-López & Mellink, 2019; Riojas-López et al., 2019).

Birds that use xeroriparian systems in the southern part of the Altiplano are little known, and the limited knowledge about them had so far derived from occasional observations only (for example, in Riojas-López & Mellink, 2019). As pointed out in the literature, intermittent and ephemeral xeroriparian systems are keystone habitats for biodiversity, although their role in Mexico has not been assessed. This keystone role can be expected to be especially important in a country like Mexico where arid and semiarid conditions cover half of its territory (Challenger, 1998). This information void precludes the design of pertinent and timely conservation plans for these habitats and the wildlife that uses them. Hence, in this study we aimed at documenting the birds that use xeroriparian systems in the highly anthropized southern part of the Altiplano, and the habitat characteristics that drive their assemblages during the non-breeding season. We studied 3 xeroriparian systems during the non-breeding bird season, with 2 objectives: 1) document the species richness, abundance and their temporal variation, and 2) determine the relationship between bird species richness and abundance and vegetation characteristics. In the context of an alarming decline of bird populations in North America (Rosenberg et al., 2019), studies like this are needed as a baseline to monitor the trends of bird populations that depend on the persistence of xeroriparian systems. The urgency of this need is increased because of the ongoing climate change in which drier and hotter regimes are predicted.

Materials and methods

The study was carried out in the Llanos de Ojuelos, at the convergence of the states of Jalisco, Zacatecas, Aguascalientes, San Luis Potosí and Guanajuato (Fig. 1). This area is a semi-arid tableland at 1,900-2,600 m altitude with a geomorphology of low mountains and valleys (Nieto-Samaniego et al., 2005). Three climatic seasons occur: dry cold (November-February), dry hot (April-May), and rainy (June to September); March and October are intermediate (Mellink et al., 2016), with an average annual temperature at the Ojuelos de Jalisco, Jalisco, meteorological station (1988-2008) of 15 °C, annual rainfall of 681 mm, and tank evaporation higher than precipitation all months of the year. The area has endorreic drainage, and rainwater flows through ephemeral streams or, in some cases, as sheet flows and collects in seasonal pools or is stored in cattle watering tanks and dams. Historically, springs were common, but the majority have disappeared (Mellink & Riojas-López, 2005).

The natural vegetation of the region is composed of grasslands (42.6% of the region’s surface), xerophilous shrublands (15.66%) and stands of dwarf oaks (Quercus spp.; 4.61%). Grasses of the genera Bouteloua, Aristida, Lycurus, and Mulhenbergia are the most common components of grasslands. Catclaws (Mimosa spp.), silver dalea (Dalea bicolor), leatherstem (Jatropha dioica), huizache (Vachellia spp.), arborescent nopales (Opuntia spp.), Peruvian pepper tree (Schinus molle), and yucca (Yucca spp.) form the shrub and arborescent layers (Harker et al., 2008; MER-L & EM pers. obs.).

Livestock and agriculture are the main productive activities in the Llanos de Ojuelos and have transformed the region´s landscape since the arrival of Spanish conquerors 450 ~ 500 years ago (Mellink & Riojas-López, 2020). Currently, approximately 35.5% of the surface of the municipalities of Ojuelos de Jalisco, Jalisco, and Pinos, Zacatecas is devoted to rain-fed farming of mostly corn, beans and fruit-oriented nopal orchards, while sheep, goats, cows, and horses graze and browse throughout the region (Pers. obs.).

Figure 1. The Llanos de Ojuelos region, southern Mexican Altiplano, indicating the 3 xeroriparian systems where bird communities were studied during the 2019-2020 non-breeding season (in white lettering), reference localities (in green upper/lowercase), and states (in green small caps).

This study was performed in 3 independent and geographically separated xeroriparian systems (localities), through visual surveying of birds during the 2019-2020 non-breeding season (Fig. 1). The localities were selected based on them being safe, accessible, and independent of each other (i.e., that their channels were not connected), and that the owners allowed us to work in them. In each system, we established 3 survey sections along the stream, with different characteristics. These xeroriparian systems, from north to south, were: La Laborcilla (Table 1). Its stream is ephemeral and flows southeast from the low mountain range that stretches between La Montesa and El Nigromante, in the municipality of Pinos. It has a straight riverbed (Sinuosity Index [SI], sensu Rosgen, 1994, < 1.1) and its slope is 8.4%. Boulders cover most of the streambed. The ground in the area adjacent to stream is mostly rocky and covered by shrubland whose major components are junipers (Juniperus deppeana), dwarf oaks, central Mexico yucca, and huisaches. The range is used for the raising of sheep and goats, along with a few cattle. Rancho Santoyo (Table 2). This is a slow-flowing straight stream (SI < 1.1), on sandy and tepetate streambed and low slope (2.4%), with permanent water in parts of it, provided by a permanent spring. The surroundings are overgrazed grassland with huisaches, and shrubland with arboreal nopales, huisaches, and pepper trees. The range is used to raise fighting-bull cattle. La Colorada (Table 3). Draining south from the Mesa del Toro, near Ojuelos, the sandy and tepetate streambed of this system is sinuous (SI = 1.1-1.3), with an overall slope of 2.3%. Its surroundings are of grasslands, some overgrazed and some in good condition, with some huisaches and shrubby nopales, and farmland. The range is used mostly for the raising of fine horses, while the nearby farmland is used to grow beans and chilies.

Table 1

Morphological characteristics and vegetation composition, based on the most common tree and shrub species of different sections of the xeroriparian system of La Laborcilla, in the Llanos de Ojuelos, southern part of the Mexican Altiplano, whose birds were studied during the 2019-2020 non-breeding season. Streambed values are mean ± standard error.

Section	Coordinates	Streambed	Description
	Lat./Long.	Width (m)	Depth (m)
Upper	22°5’32”-101°43’33”	25.8 ± 2.2	10.2 ± 2.2	A deep ravine with dwarf oaks (Quercus spp.) and junipers (Juniperus deppeana), with dispersed maguey (Agave sp.) and sotol plants (Dasylirion spp.).
Middle	22°5’26”-101°43’27”	26.1 ± 0.5	10.6 ± 1.0	A deep ravine, but here the dominant treelike form were junipers and huizaches (Vachellia spp.), with dispersed maguey and sotol plants.
Lower	22°5’17”-101°43’4”	25.0 ± 3.9	2.4 ± 0.5	A shallow ravine whose main arboreal component were junipers, with interspersed yuccas (Yucca spp.), and a shrub layer composed of dispersed leatherstem (Jatropha dioica), jimmyweed (Isocoma spp.), and catclaws (Mimosa spp.).

We surveyed the birds monthly from September 2019 to March 2020, covering the entire non-breeding season: the migratory seasons of Autumn and Spring, as well as the Winter in-between. Birds were identified and counted for 3 consecutive days at each study system, once per month. Bird inventorying was carried out for 2 hours in the afternoon ending at sunset and 2 hours the following morning starting at sunrise, as these are the periods of highest bird activity. Bird nomenclature and taxonomic arrangement follows Chesser et al. (2023).

Table 2

Morphological characteristics and vegetation composition, based on the most common tree and shrub species of different sections of the xeroriparian system of Rancho Santoyo, in the Llanos de Ojuelos, southern part of the Mexican Altiplano, whose birds were studied during the 2019-2020 non-breeding season. Streambed values are mean ± standard error.

Section	Coordinates	Streambed	Description
	Lat./Long.	Width (m)	Depth (m)
Upper	21°55’1”-101°47’32”	50.9 ± 2.5	3.8 ± 0.3	A relatively wide and moderately deep riverbead, densely vegetated with tall willows (Salix bonplandiana), cottonwoods (Populus fremontii) in addition to pepper trees (Schinus molle) and huizaches, interspersed with patches of ragwort (Senecio spp.).
Middle	21°55’10”-101°47’31”	38.0 ± 2.6	1.7 ± 0.5	A wide and shallow part of the riverbed, covered by peppertrees and ragwort.
Lower	21°55’40”-101°47’25”	12.4 ± 1.5	0.7 ± 0.5	A very thin and shallow canal, flanked by large peppertrees, with huisaches, and some catclaw and low nopales (Opuntia spp.).

Table 3

Morphological characteristics and vegetation composition, based on the most common tree and shrub species of different sections of the xeroriparian system of La Colorada, in the Llanos de Ojuelos, southern part of the Mexican Altiplano, whose birds were studied during the 2019-2020 non-breeding season. Streambed values are mean ± standard error.

Section	Coordinates	Streambed	Description
	Lat./Long.	Width (m)	Depth (m)
Upper	21°47’48”-101°38’18”	36.1 ± 5.9	4.3 ± 0.9	A deep canyon in which the most notorious trees were dwarf oaks, with dispersed catclaws and sotol, as the most abundant shrubs.
Middle	21°47’30”-101°37’34”	75 ± 5.7	6.3 ± 0.8	Semi-open deep riverbed dominated by pepper trees, with some dispersed huisaches, arborescent nopales, and willows; the most notorious shrubs were ragworts.
Lower	21°47’5”-101°36’51”	61.0 ± 8.3	7.0 ± 2.2	A semi-open riverbed in which the most notorious trees were pepper trees and arborescent nopales, with some huisaches. The most visible shrubs were catclaws, some sedges and some shrubby nopales.

Three survey stations were established in each of the 3 sections within each xeroriparian system, 40 m apart from each other and each consisting of one survey point in the center of the riverbed and 1 at the edge of the riparian habitat, looking at it. These 2 survey points allowed us to record birds that prefer the outer canopy as well as those that prefer the understory. One “day” of observation consisted of an afternoon and the following morning. We randomized the order in which the survey points were surveyed in such a way that each section was surveyed on 1 day in the first place, on 1 day in the second place, and on 1 day in the third place. For example, on day 1 survey order could be B1 [section B, station 1], A2, C3; on day 2 C1, B2, A1; and on day 3: A3, C2, B3. In some cases, riverbed survey points became darker sooner in the afternoon and lighter in the morning. Therefore, the riverbed points were surveyed before their corresponding outside station in the afternoon, and after it in the morning. Within a survey month, the same randomization was applied to the 3 xeroriparian systems, but a new randomization was performed every month. Survey order of xeroriparian systems followed logistic considerations and varied between months.

Birds at each survey point were identified and counted with 8×40 binoculars in a circle with a 20-m radius for 10 min (Brand et al., 2008; Merrit & Bateman, 2012). We did not include the birds that were observed outside or flying over the riparian system. As the best proxy of each species’ abundance in any given station we selected the highest count among the 4 counts carried out on a visit: riverbed and outside survey points, afternoon, and morning counts (Merrit & Bateman, 2012). For each section, the monthly estimate of abundance for each species was the sum of the 3 stations’ maximum values. Trophic guild and residency status of each bird species were obtained from the “The Birds of the World” series of monographs (https://birdsoftheworld.org/bow/home).

Additional to bird surveys, we measured vegetation attributes that according to the literature are important for birds (Brand et al., 2008; Powell & Steidl, 2015; Rotenberry, 1985; Wiens & Rotenberry, 1981). On 1 visit, we identified the dominant plants and measured the minimum and maximum height of shrubs and of trees. On each survey period, we determined herb cover of the ground, herb vertical density, and canopy cover. Herb cover of the ground in the region grows explosively as a result of Summer rains and dries after maturation. We used a simple scoring of 3 levels of ground cover by herbs: completely bare or nearly so, medium cover, and completely covered, or nearly so based on visual appreciation.

Herb vertical density was calculated with a 30-cm wide board divided into bands every 25 cm in height until 100 cm (0-25, 25-50, 50-75 and 75-100 cm). This board was placed 10 m away from each internal survey point in 4 directions, 2 parallel and 2 perpendicular to the streambed, and the percentage of visual obstruction in each band as seen from the center point was recorded (Hays et al., 1981).

Canopy cover was determined by foliage cover in 4 photographs of the canopy with an inclination of 30° from the vertical, at all streambed points. Two photographs were taken along the stream axis and 2 perpendicular to it, 1 to each side. The percentage of obstruction of the vegetation in each photograph was calculated counting number of pixels with and without vegetation using Photoshop ver. 2017.

Through an information-theoretic approach (Burnham & Anderson, 2002), we tested the effect of xeroriparian system and season (fixed effects) on richness, overall abundance, and abundance of the bird species that summed more than 10 individuals. Poisson distribution was used, and survey section was included as a random effect. We selected the best model with Akaike Information Criterion for small samples (AICc), applying the principle of parsimony when differences in AICc values were < 2.5 (Burnham & Anderson, 2002). Whenever we refer to a “best model” it implies that it was either the best or the most parsimonious model. We also used the same approach to explore the influence of vegetation attributes on the same bird variables. Before running the models, we obtained correlations between habitat variables and averaged those that were correlated > 0.85 and reviewed the new correlation values. This procedure was used to prevent any important variable for the birds from going unnoticed by not being part of the best model as a result of the variance that it would explain being partially accounted for by another, highly correlated variable which was included in such model. The final list of explanatory habitat variables included density of herbs, visual obstruction at 0-0.25 cm, 25-75 cm and 75-100 cm, minimum height of shrubs, minimum height of trees, mean and maximum height of shrubs and trees averaged, and canopy cover. Modeling was performed using pgirmess and lme4 libraries in R 3.3.1, through RStudio Ver. 1.2.5019.

Averaged vegetation characteristics were compared between systems through analyses of variance, followed by post-hoc Tuckey tests if statistical differences were detected (p ≤ 0.05). Similarity between systems was calculated through Jaccard´s index. We arranged study sections through Principal Components Analysis (PCA) based on their birds, both on binary data (species presence/absence) and on their abundance. These analyses were done using PAST 4.03 (https://folk.universitetetioslo.no/ohammer/past).

Results

During our surveys we identified 48 species of birds, in addition to some individuals that were identified only at genus or family level, but which likely belonged to 1 of the identified species (Supplementary material 1, 2). The identified species included 30 resident and 18 migratory bird species. Twelve additional species were recorded using xeroriparian systems, but outside our surveys. The total count during surveys was 932 individuals. Spizella passerina was the most abundant species with 149 individuals (16% of total abundance). Five other species contributed between 5 and 10% of the total abundance: Corthylio calendula, Setophaga coronata, Zenaida asiatica, Psaltriparus minimus, and Aphelocoma woodhouseii (Supplementary material 2).

Figure 2. Overall abundance (number of individuals) of bird guilds in the Llanos de Ojuelos region, southern Mexican Altiplano, during the 2019-2020 non-breeding season in 3 xeroriparian systems.

Figure 3. Monthly abundance of all birds and birds of resident species that included survey month as part of best models exploring the influence of locality (xeroriparian system) and month, during the 2019-2020 non-breeding season in 3 xeroriparian systems in the Llanos de Ojuelos, southern Mexican Altiplano.

Figure 4. Monthly abundance of birds of migrant species that included survey month as part of best models exploring the influence of locality (xeroriparian system) and month, during the 2019-2020 non-breeding season in 3 xeroriparian systems in the Llanos de Ojuelos, southern Mexican Altiplano.

Figure 5. Total abundance of species that had location as part of the best model exploring the influence of locality and survey month, during the 2019-2020 non-breeding season in each of 3 xeroriparian systems in the Llanos de Ojuelos, southern Mexican Altiplano.

La Laborcilla had a total bird count of 213 individuals (162 of 13 resident/breeding species, 48 of 8 migrant species, and 3 of 2 unidentified species), Rancho Santoyo had 353 (197/22, 149/11, and 7/3), and La Colorada, 366 (228/27, 128/16, and 10/3). Most individuals counted were of resident species or of 1 Summer (breeding) resident species (Myiarchus cinerascens),while migrants were a smaller component of the community (Fig. 2). For species richness, the best model did not include locality nor month. The best model explaining overall bird abundance included month (Supplementary material 3), but not locality. Abundance increased from Autumn (September) to Spring (March) with some differences between guilds. Insectivore migrants increased in number into the Winter and then decreased, while granivore migrants began to arrive in December and increased until March (Fig. 2). In all these cases the month of survey was part of the best model, as it was of 11 bird species (Figs. 3, 4; Supplementary material 3). Locality was part of the best model explaining abundance in 4 cases out of 27, all of them individual species (Fig. 5; Supplementary material 3). Aphelocoma woodhouseii and Leiothlypis celata were the only 2 species whose best model included both locality and moth, while the best models for the other species did not include either variable (Supplementary material 3).

Figure 6. Total abundance of birds in different trophic guilds in 3 xeroriparian systems and 3 sections within each, during the 2019-2020 non-breeding season in the Llanos de Ojuelos, southern Mexican Altiplano. Numbers on the circles indicate richness and total abundance, while numbers on the side of the dendrograph indicate similarity between xeroriparian systems, Bird assemblages in Rancho Santoyo and La Colorada were more similar between them than to La Laborcilla (Fig. 6). In PCA graphs, the 3 sections at La Laborcilla grouped closer to each other than those of the other systems. The sections within each system grouped discreetly when binary data was used (Fig. 7 top), but groups overlapped when based on abundance (Fig. 7 bottom). The 3 systems studied differed in the resident/breeding vs. migrant composition of the communities, and sections within systems were also different (Fig. 6). Whereas Rancho Santoyo had a higher proportion of insectivore migrants than the other locations, La Colorada had a higher count of granivore migrants, and La Laborcilla had proportionally more individuals of resident species (Myiarchus cinerascens did not occur in La Laborcilla). In neither case did such patterns occur in the 3 sections of the corresponding system, but only in 2 of Rancho Santoyo’s sections and in 1 and partially in another at La Colorada.

Figure 7. Principal Component arrangement of 3 study sections in each of 3 xeroriparian systems based on their bird composition during the 2019-2020 non-breeding season in the Llanos de Ojuelos, southern Mexican Altiplano. The upper figure is based on binary data (presence/absence of species), and the lower figure, on bird abundance. Ellipses were drawn around the 3 sections of each system by hand. The legends “Up”, “Md”, and “Lw” indicate the upper, middle and lower sections of each system.

The attributes of the plant communities were different between xeroriparian systems (Table 4). La Laborcilla had significantly less ground covered by herbs, whereas Rancho Santoyo and La Colorada were not different in this aspect. La Colorada had significantly denser vegetation from 0 to 75 cm above the ground than the 2 other systems, but visual obstruction at 75-100 cm was not different between the 3 systems. The tallest shrubs and highest trees were significantly taller in Rancho Santoyo than in La Laborcilla, whereas La Colorada was not different from either, and average height both shrubs and trees was significantly greater at Rancho Santoyo than at La Laborcilla, with La Colorada being in between and statistically different from either. Canopy cover was not different between systems. Study sections were all peculiar within the systems, but only in some cases were sections significantly different (Supplementary material 4). Despite slight differences, visual obstruction at the 4 heights assessed was highest in September and October, and then decreased towards their lowest values in March (Fig. 8).

At least 1 habitat attribute was part of the best bird model in all but 3 cases (Tables 5-7), the 3 of them resident species: Zenaida asiatica, Thryomanes bewickii, and Phainopepla nitens. In all cases in which canopy cover was part of the best model, it had a negative effect on bird richness or abundance, while herb density and visual obstruction at 25-75 cm had a negative effect in most of the best models that included them (Tables 5-7). In contrast, visual obstruction at 75-100 cm and mean/maximum height of shrubs/trees had a positive effect.

Figure 8. Mean visual obstruction in 4 25-cm vertical layers, between 0 and 100 cm above the ground across 3 sections in each of 3 xeroriparian systems studied during the 2019-2020 non-breeding season in the Llanos de Ojuelos, southern Mexican Altiplano. To reflect the spatial arrangement of the information, the panels are arranged bottom to top. The height stratum to which each graph corresponds is indicated on the graph. Points on each graph with the same letter are not statistically different (p < 0.05).

Discussion

The lack of studies about the role of ephemeral and intermittent xeroriparian systems as key habitats for biodiversity conservation and potential provision of ecological services severely impairs the capability of designing and implementing timely and informed conservation actions. In this study we generated a basic understanding about the composition of bird assemblages in 3 Mexican xeroriparian systems and the habitat attributes that influence them. Our study is particularly pertinent as the results of only 3 other research projects on birds in Mexican xeroriparian systems have been published (Arizmendi et al., 2008; Hinojosa-Huerta et al., 2013; Pérez-Amezola et al., 2020), none of them including ephemeral systems.

The 48 terrestrial species that we recorded represent 20% of all potential terrestrial native birds of the area, excluding swifts (family Apodidae) (based on Howell and Webb [1995]). This is relevant considering that xeroriparian systems, in general, occupy around 5% of the total land surface in western North America (Krueper, 2000), and that those we studied covered approximately 0.1% of the area in which they are located (by delineating them in Google Earth and measuring their area as well as that of the displayed image). According to Partners of Flight (2023) Campylorhynchus brunneicapillus, Spizella atrogularis, Selasphorus rufus/sasin, and Cardellina pusilla have conservation problems, while Accipiter striatus and A. cooperii are protected by Mexican law (Semarnat, 2010). The importance of xeroriparian systems in the region studied is enhanced by the fact that some otherwise woodland bird species largely depend on them, and we have not documented them in any other xeric habitats of the region (Mellink et al., 2016, 2017; Riojas-López & Mellink, 2019; Riojas-López et al., 2019).

Table 4

Vegetation attributes of 3 xeroriparian systems in the Llanos de Ojuelos, southern part of the Mexican Plateau, 2019-2020. Values are estimate ± standard error, except on maximum and minimum heights. Values of any variable with different literal were significantly different (p ≤ 0.05) according to an ANOVA + Tukey post hoc tests. Superscript ^“ns” indicates that the means were not significantly different.

Site/section

Herb

Visual obstruction (%)

Hight of shrubs (m)

Height of trees (m)

Canopy

density (1-4)

0-25 cm

25-50 cm

50-75 cm

75-100 cm

Max

Min

Mean

Max

Min

Mean

cover (%)

La Laborcilla

1.53 ± 0.38^b

12.00 ± 4.27^b

4.22 ± 2.58^b

0.89 ± 1.06^b

0.40 ± 0.55^ns

2.63 ± 0.32^b

0.23 ± 0.10^ns

0.63 ± 0.01^c

8.37 ± 0.27^b

0.73 ± 0.26^ns

3.58 ± 0.26^c

40.40 ± 8.82^ns

Rancho Santoyo

2.52 ± 0.88^a

13.60 ± 16.7^b

3.03 ± 4.75^b

0.85 ± 2.38^b

0.83 ± 2.27^ns

3.55 ± 0.49^a

0.31 ± 0.08^ns

1.41 ± 0.31^a

14.65 ± 3.04^a

1.20 ± 0.44^ns

4.79 ± 0.89^a

39.50 ± 16.83^ns

La Colorada

2.70 ± 0.95^a

35.98 ± 17.06^a

16.04 ± 10.83^a

6.40 ± 6.32^a

1.59 ± 2.48^ns

3.14 ±0.76^ab

0.22 ± 0.06^ns

1.21 ± 0.44^b

10.36 ± 3.55^ab

0.87 ± 0.19^ns

4.54 ± 0.54^b

45.48 ±29.86^ns

These species can be considered locally xeroriparian-dependent. They are Accipiter striatus, A. cooperii, Empidonax difficilis occidentalis, Pitangus sulphuratus, Empidonax wrightii, Corthylio calendula, Turdus migratorius, Setophaga coronata, Setophaga townsendi, Piranga ludoviciana, Bubo virginianus, Sphyrapicus varius, and Cardinalis cardinalis. This was also the case of Pipilo maculatus and P. chlorurus, otherwise species of thick shrublands. The system with more xeroriparian-dependent species was La Colorada (9 species) followed by Santoyo (7) and La Laborcilla (6). However, Santoyo had more riparian-dependent individuals (139) than La Colorada (78) and La Laborcilla (45), Setophaga coronata and Corthylio calendula being the most abundant species (Supplementary material 2).

Table 5

Sign of the effects of habitat features on the bird community variables in 3 study sections in each of 3 xeroriparian systems studied during the 2019-2020 non-breeding season in the Llanos de Ojuelos, southern Mexican Altiplano. The only data indicated are that of variables included in the best or more parsimonious model under an information-theoretic approach. Blank cells are of variables not included in such models. Min. indicates minimum, and Max., maximum. Variables with correlation coefficients > 0.85 were merged before the analysis. The intercept is not shown. Actual data is presented in Supplementary material 5.

Bird community variable	Herb	Visual obstruction (%)	Shrub Min.	Tree Min.	Shrub-tree	Canopy
	Density (1-4)	0-0.25 cm	25-75 cm	75-100 cm	Height (m)	Height (m)	Min./Max. (m)	Cover (%)
Richness							+	–
Abundance
Overall	–		–	+				–
All resident species	–		–					–
All migrants			–	+			+
Migrant insectivorous birds		–					+	–
Migrant granivorous birds			–	+				–

Table 6

Sign of the effects of habitat features on the abundance of resident species of birds in 3 study sections in each of 3 xeroriparian systems studied during the 2019-2020 non-breeding season in the Llanos de Ojuelos, southern Mexican Altiplano. The only data indicated are that of variables included in the best or more parsimonious model, under an information-theoretic approach. Blank cells are of variables not included in such models. Min. indicates minimum, and Max., maximum. Variables with correlation coefficients > 0.85 were merged before the analysis. The intercept is not shown. Actual data is presented in Supplementary material 5.

Bird response variable	Herb	Visual obstruction (%)	Shrub Min.	Tree Min.	Shrub-tree	Canopy
	Density (1-4)	0-0.25 cm	25-75 cm	75-100 cm	Height (m)	Height (m)	Min./Max. (m)	Cover (%)
Zenaida asiatica
Melanerpes aurifrons								–
Sayornis nigricans							+
Aphelocoma woodhouseii			–				–
Psaltriparus minimus	–	+	–					–
Phainopepla nitens
Thryomanes bewickii
Mimus polyglottos							+
Spinus psaltria			+		+	+	–
Spizella passerina	–		–					–
Melozone fusca							+
Pipilo maculatus						–	+	–

Table 7

Sign of the effects of habitat features on the abundance of migratory birds in 3 study sections in each of 3 xeroriparian systems studied during the 2019-2020 non-breeding season in the Llanos de Ojuelos, southern Mexican Altiplano. The only data indicated are that of variables included in the best or more parsimonious model, under an information-theoretic approach. Blank cells are of variables not included in such models. Min. indicates minimum, and Max., maximum. Variables with correlation coefficients > 0.85 were merged before the analysis. The intercept is not shown. Actual data is presented in Supplementary material 5.

Bird response variable	Herb	Visual obstruction (%)	Shrub Min.	Tree Min.	Shrub-tree	Canopy
	Density (1-4)	0-0.25 cm	25-75 cm	75-100 cm	Height (m)	Height (m)	Min./Max. (m)	Cover (%)
Empidonax wrightii						+
Corthylio calendula	–						+
Troglodytes aedon	+
Turdus migratorius			–			–	+	–
Melospiza lincolnii			–			–	+	–
Spizella pallida			–	+		–	+	–
Leiothlypis celata	+
Setophaga coronata		–
Cardellina pusilla							+

Resident species increased their abundance from December through March (Figs. 2, 3), a pattern that could have been driven by 3 processes, not necessarily mutually exclusive: 1) resident species that might breed in xeroriparian habitats disperse to feed in other habitats in the region after nesting, might have begun to congregate for the upcoming breeding season, which would make the different habitats complementary (Dunning et al., 1992); 2) species like the P. maculatus might become more detectable as breeding-associated territoriality and courting behaviors develop; 3) migrating individuals of northern populations of species that locally remain resident might pass through the region in the Spring (perhaps S. passerina; Fig. 4).

The increase in abundance of the resident species as the season progressed was combined with the addition of migratory species in their northbound Winter-Spring migration. The pattern observed in our study is similar to that in the lower Colorado River in southwestern Arizona, where more birds migrate during the Spring than during the Autumn and suggests that some species migrate via different routes and/or use different habitats during the latter (Carlisle et al., 2009). According to our data, the region is part of the Spring migration route, but not, or less so, of the Autumn route.

Birds assemble differently in response to habitat characteristics (Wiens & Rotenberry, 1981), although bird-habitat relationships are complex (Strong & Bock, 1990). In our study, habitat characteristics were part of the best model in 78% of the cases (Tables 5-7). Three habitat variables more consistently affected bird assemblages and species. The first was that the averaged minimum and maximum height of shrubs and trees influenced birds positively, which conforms with general known principles in bird ecology (Brand et al., 2008; MacArthur & MacArthur, 1961; Merrit & Bateman, 2012; Rockwell & Stephen, 2018), and with findings in other xeroriparian systems (Brand et al., 2008). The second was that closed canopies had a negative effect. Closed canopies have been found to influence birds negatively by reducing light at ground level resulting in a less developed herb and shrub community (Beedy, 1981). The third case was that herb vertical density at 25-75 cm had also a negative effect. But this is a spurious outcome that resulted from the dense herb layer at the beginning of the study (Fig. 8), when bird abundance variables were lower, while the circannual process of herbs drying and decaying in the late Autumn and early Winter causes low herb cover coinciding with the increase in bird abundance (Figs. 2, 3).

The bird assemblages of the xeroriparian systems studied not only were different from each other, but also varied internally, between sections (Figs. 6, 7). The arrangement of the 9 sections according to their species presence/absence in axis 1, explaining 33% of the variance, follows a clear gradient (Fig. 7 top). On the left side are sections with steep, narrow, and rocky ravines with large boulders, dominated by oaks and junipers that form a close canopy with little understory herbaceous vegetation. On the right, wide and open pebbled washes, dominated by a more heterogeneous tree community composed of peppertrees, arborescent nopales, and huisaches, with a well-developed herbaceous layer. The bird communities responded to this gradient with increasing richness and abundance from left to right.

In the same graph, axis 2 follows a gradient from a well-developed shrub community and abundant litter and wetter soil to no or scarce shrubs with a dense herbaceous layer and drier ground. This gradient apparently drives the food resources available to birds, as suggested by the preponderant bird guilds in the different sections (Fig. 6): insects in its lower end to seeds in the upper end. Overall, La Colorada with the most heterogeneous sections, vegetation-wise, had also the richest bird assemblage, while La Laborcilla, with the most homogenous sections, had the poorest one, with Rancho Santoyo intermediate in both attributes (Table 4; Fig. 6; Supplementary material 5). Using bird abundance instead of binary information rearranged the PCA graph layout (Fig. 7 lower) because of the effect of species that were widespread and abundant, but without losing a resemblance to the species presence/absence PCA.

Vertical structure is important for birds, but floristic composition can also influence their diversity (Fleishman et al., 2003; Rotenberry, 1985). For example, oaks are of little attraction to most birds (Powell & Steidl, 2015), and their dominance at La Laborcilla and the upper section of La Colorada coincided with the lower richness and abundance of their bird assemblages (Fig. 6; Supplementary material 2). Rancho Santoyo supported more xeroriparian-dependent individuals, mostly of Setophaga coronata and Corthylio calendula, both small insectivorous birds. The middle and upper sections where these 2 species thrived had large cottonwoods (Populus fremontii) and willows (Salix bonplandiana). In contrast, in the middle section of La Colorada, which also had tall trees but were peppertrees and arborescent nopales, these 2 bird species were much less abundant.

Each of the systems studied had a distinct signature given by one species or dominant bird guild(s), although such signature was largely due to the assemblages in the individual sections (Fig. 6). The signature species at Laborcilla was Aphelocoma woodhouseii, whose primary habitat includes oak and juniper forests, where it typically feeds on juniper berries in the Autumn and Winter (Fig. 5; Cornell Lab of Ornithology, 2019). Although the upper Colorada section grouped with La Laborcilla, with which it shared oaks, lacked junipers and was not used by Aphelocoma woodhouseii. Their close PCA grouping rather resulted from their shared poor bird assemblages. Rancho Santoyo can be identified with migrant insectivorous birds and La Colorada with migrant granivorous birds, in concordance with the explanation on the PCA arrangement provided above.

The lower proportion and abundance of migratory insectivorous birds and absence of granivorous birds at La Laborcilla might have been caused by its less developed understory vegetation and enclosed canyon conditions. In contrast, Rancho Santoyo´s upper and middle section provided the best habitat for insectivore migrants. This system was exuberant in herb and shrub foliage, likely as a result of the longer presence of ground humidity, but had also plenty of sunny spots; and the system bordered open rangeland, providing lengthy, sharp borders, especially in its upper and middle sections. Granivore migrants were a small component of the communities we documented, and they were present almost exclusively in La Colorada´s middle section. This site had an open canopy and combined taller shrubs with denser and taller herbs than in the other sections of the same and the 2 other systems, providing higher habitat heterogeneity and, likely, more seeds. A more developed herb-shrub stratum at 0-75 cm at La Colorada than at other sites provided good escape cover adjacent to open patches that provided seeds (Table 4; Supplementary material 4).

As our data exhibit, habitats associated with non-perennial xeroriparian streams are far from uniform, not only between systems but also within them. At a landscape level they are clearly keystone structures, at least for the birds but surely for other groups as well, both collectively and individually. The 3 systems studied by us cover about 55 ha, roughly 0.1% of the area in which they occur. However, they supported 20% of the potential species of terrestrial birds of the region, including 15 that we have recorded only in such riparian habitat. Our data exhibit that in addition to their importance for resident species, some ephemeral and intermittent xeroriparian habitat in the southern part of the Mexican Altiplano are important for northbound Spring migrating birds.

Our study is a first approximation to the ecological role of xeroriparian systems in the region. However, many issues, like their importance as nesting habitat, provision of food, climatic protection, interaction with adjacent and farther away habitats, among others, remain to be studied. Nevertheless, if these xeroriparian habitats disappear, regional biodiversity would be impacted. Not only 1 or a few, but many or all xeroriparian systems, and their different sections in the region studied by us should be targeted for conservation management. Xeroriparian systems have long been considered important elements of the landscape and their conservation needs recognized. However, such consideration, and the actions derived from it, usually focus on perennial streams with their lush arboreal communities. This focus is biased and excludes an important part of xeroriparian habitat: that created by ephemeral and intermittent streams. Despite their low consideration in research and in conservation agendas, as our study and a few others have demonstrated, ephemeral and intermittent xeroriparian habitat can play a crucial role in arid and semiarid lands (Johnson & Haight, 1985; Levick et al., 2008; Sánchez-Montoya et al., 2017; Szaro & Jakle, 1985). Despite covering less than 0.1% of the region´s area, in our study they supported 20% of all terrestrial species that we documented in the region (Mellink et al., 2016, 2017; Riojas-López & Mellink, 2019; Riojas-López et al., 2019), while those that we documented only in xeroriparian systems account for 9% of all species documented. A scenario of ecological importance of non-perennial xeroriparian systems and research and management neglect are likely to occur in many other arid and semiarid regions of the world. Hence, it might be time to join forces and impulse a global agenda for their conservation, which is now especially pertinent in view of the ongoing climate change in which drier and hotter regimes are predicted.

Acknowledgements

Jaime Luévano Esparza, David H. Almanzor, Santiago Cortés, and Marco A. Carrasco assisted during field work. Access and research permission were granted kindly by owners Family Santoyo (Rancho Santoyo) and Enrique Campos (La Laborcilla), and ranch manager Melquíades Contreras (La Colorada). Ezequiel Martínez and Margarita Chávez provided logistic support. Two anonymous reviewers provided extensive and valuable comments. Our greatest appreciation to all of them. Financial support was provided by the Centro de Investigación Científica y de Educación Superior de Ensenada (CICESE), the Universidad de Guadalajara, and the first two authors´ personal funds. The Consejo Nacional de Humanidades, Ciencias y Tecnologías supported MM-O through a M.Sc. scholarship.

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2937305

Don’t count your eggs before they hatch: differential survival of artificial bird nests in an anthropogenically modified landscape in western Mexico

PDF

Dallas R. Levey ^{a, b}, Ian MacGregor-Fors ^c,*

^aStanford University, Department of Biology, 327 Campus Drive, Stanford, California, 94305 USA

^bUniversidad Nacional Autónoma de México, Instituto de Biología, Tercer Circuito s/n, Ciudad Universitaria, Coyoacán, 04510 Mexico City, Mexico

^cUniversity of Helsinki, Faculty of Biological and Environmental Sciences, Ecosystems and Environment Research Programme, Niemenkatu 73, FI-15140, Lahti, Finland

*Corresponding author: ian.macgregor@helsinki.fi (I. MacGregor-Fors)

Received: 19 October 2023; accepted: 1 February 2024

Abstract

Native habitat conversion to urban and agricultural areas represents conservation concerns for habitat quality and the breeding success of birds. In tropical areas facing regular deforestation of at-risk habitats, changes may occur to bird and nest predator communities that influence contradictory trends in breeding success. To assess the value of working lands for birds, we placed 100 artificial nests in 5 habitat types of varying human footprint, including a tropical dry forest reserve, a biological research station, croplands, and 2 urban towns. We report a clear decline in survival from the forest to urban towns. Habitat type explained the variation in nest survival probabilities over nest height, elevation, or time of nest exposure. Reducing the structural and compositional contrast of habitat and landscape vegetation between tropical dry forest and working lands represent valuable conservation actions for increasing habitat quality for birds.

Keywords: Croplands; Bird nest predation; Habitat quality; Jalisco; Plasticine eggs; Tropical dry forest; Urbanization

(http://creativecommons.org/licenses/by-nc-nd/4.0/).

No cuentes los huevos antes de que eclosionen: supervivencia diferencial de nidos artificiales de aves en un paisaje antropogénicamente modificado en el oeste de México

Resumen

La conversión de hábitats nativos en áreas urbanas y campos agrícolas representa problemas de conservación para la calidad del hábitat y el éxito reproductivo de las aves. La deforestación constante de hábitats en riesgo puede cambiar las comunidades de aves y los depredadores de los nidos, lo que puede influir en su éxito reproductivo. Para evaluar el valor de los hábitats dentro de un paisaje antropogénicamente modificado en el éxito reproductivo de las aves, colocamos 100 nidos artificiales en 5 hábitats con diferentes niveles de actividades humanas, incluyendo una reserva de bosque tropical caducifolio, una estación de investigación biológica, campos agrícolas y 2 pueblos urbanos. Encontramos una clara disminución en la supervivencia de nidos artificiales desde el bosque tropical caducifolio hasta los pueblos urbanos. El tipo de hábitat fue la variable que mejor explicó la variación en las probabilidades de supervivencia de los nidos artificiales en comparación con la altura del nido, la elevación y el tiempo de exposición del nido. Reducir el contraste dentro del paisaje en la estructura de la vegetación entre la reserva y los hábitats dentro del paisaje modificado representan acciones de conservación importantes para aumentar la calidad del hábitat para las aves.

Palabras clave: Campos agrícolas; Depredación de nidos de aves; Calidad de hábitat; Jalisco; Huevos de plastilina; Selva seca tropical; Urbanización

Introduction

Urbanization and the conversion of native habitat to agricultural land represent key factors in the long-term conservation of bird biodiversity (Aronson et al., 2014; Kehoe et al., 2017). In the tropics, urbanization and agriculture have led to the degradation and destruction of native vegetation and the reconfiguration of landscapes, causing stark contrast in habitat complexity between remnant vegetation and agricultural and urban areas that pose risks to bird biodiversity (Filloy et al., 2019; Fischer et al., 2015; Maas et al., 2016). Biodiverse tropical regions suffer some of the highest rates of urbanization and native habitat transformation (Estrada et al., 2020), which represent pressing challenges for the conservation of bird populations.

A key component of bird biodiversity and population monitoring in tropical landscapes with high rates of natural habitat transformation includes the evaluation of breeding ecology (DeGregorio et al., 2016). Reduced vegetative complexity and the exchange of native plants with non-native plants, both common attributes of agricultural and urban areas (Chace & Walsh, 2006), tend to negatively impact bird species with highly sensitive breeding requirements tied to native vegetation (Maas et al., 2016). Vegetation change in the tropics alters biotic —e.g., nest predation pressure and reduction of nest locations— and abiotic conditions —e.g., increased nest exposure, higher temperatures, and brighter conditions—, leading to potential direct and indirect influences on avian breeding ecology in species that depend on native plants and vegetation structure for nesting (Estrada et al., 2002; Rivera-López & MacGregor-Fors, 2016; Tellería & Díaz, 1995; Zuñiga-Palacios et al., 2021). Meanwhile, certain bird species may be positively impacted by or able to acclimate to novel conditions (DeGregorio et al., 2016; Kurucz et al., 2021; Latif et al., 2012), underlining the semi-permeable ecological filter that is applied to nesting birds in human-modified tropical landscapes and the importance of evaluating bird breeding ecology in different types of transformed land (MacGregor-Fors, 2010; MacGregor-Fors et al., 2022).

Nest predation represents a powerful force on bird breeding success and population dynamics (DeGregorio et al., 2016). A consequence of native habitat conversion to more urban or agricultural areas includes changes to nest predator communities, and the ability of bird species to adapt to these changes will ultimately determine whether disturbed areas offer viable habitat for native levels of biodiversity (DeGregorio et al., 2016; Latif et al., 2012). Urban and agricultural areas tend to have lower vegetation cover as forested habitats, leading to different natural predator abundance and nest visibility to predators, representing powerful determinants of breeding success for bird species that use transformed land (López-Flores et al., 2009; Martin, 1993; Zuñiga-Palacios et al., 2021). More disturbed areas may lead to a reduction of nest predation pressure due to the absence of native nest predators that have a low tolerance for human activity (Kurucz et al., 2021; Pretelli et al., 2023). A possible caveat to lower predation pressure from typical native predators in urban areas include birds that are habitat and foraging generalists (Estrada et al., 2002; Martin, 1995; Rivera-López & MacGregor-Fors, 2016), mammals that are attracted to anthropogenic food sources (Fischer et al., 2012), and increased access to nests by people that manipulate and destroy nests and eggs (López-Flores et al., 2009).

To assess the survivorship of bird nests, we placed artificial bird nests in 5 habitat types with increasing degrees of human disturbance and habitat modification, including 1) a tropical dry forest reserve (TDF hereafter), 2) the Chamela Biological Research Station (CBRS) grounds, embedded in the Chamela-Cuixmala Biosphere Reserve, 3) croplands (CL), 4) Careyes (CAR), a small and heavily built-up town, and 5) Emiliano-Zapata (ZAP), a larger town. While a recent meta-analysis questions the efficacy of artificial nest studies in determining nest survival probabilities in urban areas relative to natural nests (Vincze et al., 2017), the feasibility of finding sufficient numbers of natural nests in heavily built-up urban areas (i.e., outside of urban parks and green spaces) makes the use of artificial nests necessary. We controlled for important variables that may influence predation rates, such as nest size and height, to focus on habitat-level variations in nest survivorship and the impacts of urban and agricultural areas in the working landscape. Such landscapes are common in the tropical areas of Mexico (Levey et al., 2023), where existing reserves are surrounded by a working landscape with non-native vegetation that contrasts highly with native areas (Levey & MacGregor-Fors, 2021; Levey et al., 2021; MacGregor-Fors & Schondube, 2011; Vázquez-Reyes et al., 2017). Efforts to evaluate the impacts on breeding ecology in these working tropical landscapes are needed to supplement a thin body of work (Estrada et al., 2002; López-Flores et al., 2009; Zuñiga-Palacios et al., 2021) and determine the risks that urban and agricultural areas present for breeding birds. We expected nest survivorship to be lower in CL, CAR, and ZAP relative to the conserved TDF reserve and the CBRS due to higher exposure of nests and greater visibility for predators due to reduced vegetation complexity and density (Estrada et al., 2002; López-Flores et al., 2009; Zuñiga-Palacios et al., 2021).

Materials and methods

We conducted our study in a landscape between the Chamela-Cuixmala Biosphere Reserve (19°29’57.5” N, 105°02’41.6” W) and the town Emiliano Zapata (19°23’16.6” N, 104°57’50.1” W) in the Municipality La Huerta (population: 23,258; INEGI, 2020) on the Pacific coast of Jalisco, Mexico (Fig. 1). Historically, native vegetation cover in the region consisted primarily of tropical dry forest, which consists of deciduous forest with a mean canopy height of 12 m, a dense understory (Rzedowski, 2006), and strong phenological changes due to highly seasonal rainfall in the region (Durán et al., 2002). Other forest types exist in areas with more regular water availability, including semi-deciduous (mean canopy height of 20 m) and mangrove forests (Durán et al., 2002). After a period of increased human occupation and agricultural expansion from 1950-1970, large cover of tropical dry forest and other native forest types in lower elevation zones were converted to small towns and agricultural lands, linked by paved and unpaved roads, creating a landscape mosaic of native and non-native vegetation types (Maass et al., 2005).

In this landscape, we selected 5 habitat types with varying degrees of urban and agricultural disturbance for artificial nest placement: 1) TDF, with closed canopy cover and dense understory, 2) CBRS, which consists of moderately built-up 1.4 ha area embedded within the Chamela-Cuixmala Biosphere Reserve, 3) CL, consisting of fields of small, herbaceous plants such as maize (Zea mays), squash (Cucurbita spp.), chili pepper (Capsicum spp.), watermelon (Citrullus lanatus), and beans (Phaseolus spp.) located in the southern edge of the study area (Maass et al., 2005), 4) CAR (19°26’36.15” N, 105°1’49.65” W), a small town with heavy built-up cover, and 5) ZAP, a large town with less built-up cover than CAR (Fig. 1). Both elevations (MSL) of the TDF and CBRS sampling areas were slightly higher than the other habitat types. The TDF and CBRS sampling areas are also in closer proximity to each other than the other sampling locations. We included both habitat categories due to the higher human presence at the Biological Station, the noise generated by people and activities at the station, and a higher density of paved roads that could influence the occupancy of bird and mammals that respond positively to increasing human footprint (Rivera-López & MacGregor-Fors, 2016). Potential bird nest predators in the study region included White-throated Magpie-jays and San Blas jays (Calocitta formosa and Cyanocorax sanblasianus), Great-tailed grackles (Quiscalus mexicanus), mammals (e.g., Nasua narica, domestic dogs and cats, rodents, possums, and Procyon lotor), and diverse reptiles.

We used a mixture of plant fibers, twigs, and mud from the nest location to create bird nests in the shape of open plant fiber nest cups large enough to hold both the clay and quail eggs. We created open cup nests since many species in the study area construct nests in similar ways (e.g., Cyanocorax sanblasianus, Peucaea ruficauda, and Turdus rufopalliatus; Mendoza-Rodríguez et al., 2010) and due to the ease of creating such a nest shape. We placed each nest ~ 2 m above ground to control the tendency of nest height placement to affect predation rates (DeGregorio et al., 2016). We placed 1 Japanese Quail (Coturnix japonica) commercial egg and 1 clay egg of similar size for a total of 2 eggs in each nest (Bayne et al., 1997; Estrada et al., 2002). We used clay since it is a malleable material that preserves markings from predation events and has negligible influence on predation rates (Bayne & Hobson, 1999; Bayne et al., 1997). We used commercial quail eggs due to their small size and color speckling that best mimicked natural terrestrial bird eggs relative to domestic chicken eggs and their availability in the study region. We used both a real and clay egg to provide stimulus for a wider range of predators than clay eggs alone and to capture predation event evidence if we could not perceive markings on the quail egg from smaller nest predators (Bayne et al., 1997; Estrada et al., 2002). We used rubber gloves to prevent leaving a human scent when handling nest materials and eggs (Estrada et al., 2002).

Figure 1. Region of study in the state of Jalisco in western Mexico. We placed artificial bird nests at the localities marked with a black dot and text, including ‘Forests’ (tropical dry forest of the Chamela-Cuixmala Biosphere Reserve), ‘Biology station’ (the Chamela Biological Research Station), ‘Cropfields’ (herbaceous crop plots), ‘Careyes’ (a small, heavily built-up town), and ‘Zapata’ (a large, less built-up town). Nest locations within the marked localities by at least 250 m to increase spatial independence.

We placed 20 artificial nests in each of the 5 habitat types for a total of 100 nests. Nests were exposed for a total of 12 days (April 30 – May 11, 2009), and we checked nests at 3-day intervals for a total of 4 nest visits. We considered nests as failed if the eggs were missing or if there were indications of a predation event on either the clay or quail egg, including scratches, bite marks, or perforations. We removed nests with signs of predation from the sample locations. We considered nests successful if there were no markings on either the clay or quail egg.

Figure 2. Survival probability with 95% confidence intervals from the Known Fate analysis in MARK of the artificial nests in the conserved tropical dry forest (TDF in the figure), Chamela Biological Research Station (CBRS), cropland (CL), the town of Careyes (CAR), and the town of Zapata (ZAP).

We used the program MARK (White & Burnham, 1999) to perform a known fate analysis using our nest check interval to calculate the probability of survivorship of each nest (Dinsmore & Dinsmore, 2007), using the covariables nest height (m), elevation (m asl), habitat type, and time of nest exposure to generate the models. We included the nest height variable in analyses despite controlling the height at 2-m to check for potential interactions with other covariates. We included elevation in our models to account for slight elevation differences between nest site locations and the tendency of lower elevation areas to have higher cover of agricultural and urban areas (Maass et al., 2005). We included habitat type to determine the differences between certain habitat types on artificial nest survival. Finally, we included the time of nest exposure since the likelihood of nest survival is tied to the amount of time eggs are exposed to predators (Dinsmore & Dinsmore, 2007). We ranked the models by parsimony using the adjusted Akaike’s Information Criterion for small sample sizes (AICc; Hurvich & Tsai, 1989). We selected the models that best fit our data by calculating the differences in AICc values (ΔAICc) and choosing those with ΔAICc values less than 2 units from the most parsimonious model (Burnham & Anderson, 2002).

Results

We recorded 82 preyed upon nests of 100 total, including 37 (45.1%) instances of bird predation, 30 (36.6%) instances of unknown predation, 10 (12.2%) instances of egg removal or manipulation by humans, 3 (3.7%) instances of rodent predation, and 2 (2.4%) instances of reptile predation. We recorded 18 nests with no predation signs, with the majority remaining in TDF (44.4%), followed by CBRS (27.8%), CL (22.2%), and ZAP (5.6%). No nests placed in CAR survived the observation period. Nest survival probability was 0.38 (95% CI: 0.26-0.48) in TDF, 0.27 (95% CI: 0.17-0.33) in CBRS, 0.25 (95% CI: 0.15-0.35) in CL, 0.06 (95% CI: 0.01-0.13) in ZAP, and 0.0 in CAR (Fig. 2). The most parsimonious model to explain the variation in nest survival probabilities included the lone covariable habitat, followed closely by the combination of habitat and height (Table 1).

Table 1

Model output from the Known Fate analysis in MARK. Covariates used in the models include habitat, nest height (controlled at 2 m above ground level), elevation, and time of nest exposure.

Model	AICc	ΔAICc	AICc weight	Model likelihood	Parameters	Deviance
Habitat	262.62	0.00	0.44	1.00	5	252.32
Habitat + height	263.96	1.35	0.22	0.51	6	251.55
Habitat + elevation	264.49	1.87	0.17	0.39	6	252.08
Habitat + height + elevation	265.90	3.29	0.09	0.19	7	251.35
Elevation	267.21	4.59	0.04	0.10	5	256.91
Height + elevation	268.74	6.12	0.02	0.05	6	256.32
Time of nest exposure	270.31	7.69	0.01	0.02	4	262.11
Height	272.26	9.64	0	0.01	5	261.96

Discussion

The impacts of bird nest predation along habitat disturbance gradients vary depending on the severity of habitat modification and the biotic and abiotic conditions of transformed land (Vincze et al., 2017). Novel biotic and abiotic conditions in urban and agricultural settings heavily contrast with native habitat, representing important influences on bird breeding success and, ultimately, biodiversity conservation (DeGregorio et al., 2016). We report a clear decline in the survival probabilities of artificial bird nests throughout a gradient of urban intensity between a conserved tropical dry forest and the largest town.

TDF, the most conserved habitat in the disturbance gradient, had the highest artificial nest survival probability among all studied habitats. This finding is consistent with other artificial nest studies from the tropical Americas that show greater vegetation cover offers increased survival odds by concealing nests more effectively from predators, both within forests with seasonal leaf cover (Vega-Rivera et al., 2009) and relative to more open areas (Estrada et al., 2002; López-Flores et al., 2009). TDF contains a dense understory of vegetation and a closed canopy with darker lighting, which may be a key factor in the detection of nests by predators (Estrada et al., 2002; Vázquez et al., 2021). While some studies have found that conserved areas either have similar or lower nest survival probabilities than in urban settings due to changes in predator abundance and composition (DeGregorio et al., 2016; Fischer et al., 2012; Zuñiga-Palacios et al., 2021), local factors in this heterogeneous landscape with various habitat types likely favor ample distribution of potential nest predators (e.g., urban birds, domesticated cats, and dogs) in urban areas (Estrada et al., 2002; López-Flores et al., 2009; Rivera-López & MacGregor-Fors, 2016).

Outside of the conserved TDF habitat, CL showed near-equal nest survival probabilities as the CBRS, which were lower than in TDF. Our results indicate that even small (< 2 ha), moderately built-up areas embedded in conserved habitat may increase the likelihood of nest predation to levels found in agricultural land. Synonymous with development is the opening of forest habitat, leading to new abiotic conditions and biotic stimulus that may influence breeding success in birds (Patten & Smith-Patten, 2012; Shochat et al., 2010). In our study area, CBRS has attracted several bird species that are opportunistic omnivores and often associated with open habitats, such as the Great-tailed Grackle (Quiscalus mexicanus; MacGregor-Fors et al., 2009). Also attracted to this habitat and CL are potential nest predators such as the White-nosed Coati (Nasua narica) and Common Raccoon (Procyon lotor), which have been documented to predate bird nests (Estrada et al., 2002; Menezes & Marini, 2017; Robinson et al., 2005). Snakes, which occur at similar compositions inside and outside the reserve, may exhibit increased activity at edge habitats (Chalfoun et al., 2002; Suazo-Ortuño et al., 2008; Vetter et al., 2013). These changes to the nest predator communities in CBRS and CL could have important implications on bird breeding success (DeGregorio et al., 2016), and continued urbanization of these areas may continue to decrease nest survival probabilities to the levels of heavily built-up towns.

The built-up areas along the urbanization gradient in our study had significantly lower nest survival probabilities than the other studied habitats. Urbanization and loss of native vegetation have been shown to negatively influence the survival of bird nests in previous studies (Rivera-López & MacGregor-Fors, 2016; Thorington & Bowman, 2003), and a potential mechanism includes the introduction of novel predation pressures, such as domesticated cats (Patterson et al., 2016), dogs (Zuñiga-Palacios et al., 2021) and humans (López-Flores et al., 2009). While it has been shown that urban areas may increase nest survival and breeding success in birds (Fischer et al., 2012; Kurucz et al., 2021), the urban areas in our study area presented an overwhelming amount of novel predation pressures that are not present in the other studied habitats (Chace & Walsh, 2006; López-Flores et al., 2009), highlighting the importance of evaluating changes in the communities of bird nest predators along habitat disturbance gradients (DeGregorio et al., 2016). Conserving and restoring degraded areas within working landscapes and urban centers through measures such as live fencing, remnant forest preservation, and educational programs on bird breeding ecology may provide vital nesting habitat and increase bird breeding success (Bocz et al., 2017; Zuñiga-Palacios et al., 2021).

Acknowledgements

We thank the Estación de Biología Chamela (Instituto de Biología, UNAM) for granting permission to place artificial nests in the biosphere reserve. We thank Carlos Lara for editing and three anonymous reviewers for comments that enhanced the quality and clarity of the manuscript. We thank Michelle García-Arroyo for creating the study area map. DRL received a Master’s scholarship from Conahcyt (grant number 964233) as part of the Posgrado en Ciencias Biológicas of the Universidad Nacional Autónoma de México.

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Ringtails (Bassariscus astutus) as seed dispersers in an urban gradient under conditions of low human activity due to COVID-19

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Joselin Judith Peña-Herrera ^a, Yury Glebskiy ^{a, b,} *, Teresa de Jesús Hernández-Trejo ^a, Zenón Cano-Santana ^a

^a Universidad Nacional Autónoma de México, Facultad de Ciencias, Departamento de Ecología y Recursos Naturales, Laboratorio de Interacciones y Procesos Ecológicos, Circuito Exterior s/n, Ciudad Universitaria, Coyoacán, 04510 Ciudad de México, Mexico

^b Universidad Nacional Autónoma de México, Facultad de Ciencias, Posgrado en Ciencias Biológicas, Circuito Exterior s/n, Ciudad Universitaria, Coyoacán, 04510 Ciudad de México, Mexico

*Corresponding author: agloti@ciencias.unam.mx (Y. Glebskiy)

Received: 14 September 2023; accepted: 6 March 2024

Abstract

Seed dispersal by animals is a key ecosystemic process in many environments; however, it could be compromised or increased in urban environments due to changes in the landscape, the introduction of exotic species, and human activities. This article aims to evaluate the role of ringtails (Bassariscus astutus) as seed dispersers in an urban-natural gradient during low human activity due to the COVID-19 pandemic. Ringtail feces were collected in 3 sampling sites with different levels of urbanization (ranging from 100 to 5% of natural vegetation), and the seeds germinated in germination chambers. Twenty species of plants were dispersed by ringtails, more than reported in previous studies. More seeds were dispersed in natural (7.1 seeds per g) than urbanized (3.2 seeds per g) areas, but diversity and richness were higher in urbanized areas. This suggests that urban environments have a greater diversity, and it could be attributed to the microenvironments created by urban infrastructure and the exotic plants that are established in the area.

Keywords: Endozoochory; Mexico City; Opuntia; REPSA; Zoochory

(http://creativecommons.org/licenses/by-nc-nd/4.0/).

Cacomixtles (Bassariscus astutus) como dispersores de semillas en un gradiente urbano bajo condiciones de baja actividad humana por COVID-19

Resumen

La dispersión de semillas por animales es un proceso clave en muchos ecosistemas, pero este se puede ver comprometido o incrementado en ambientes urbanos debido a cambios en el paisaje, introducción de especies exóticas y actividades humanas. El objetivo de este artículo es evaluar el papel del cacomixtle (Bassariscus astutus) como dispersor de semillas en un gradiente urbano-natural durante un periodo de baja actividad humana debido a la pandemia de COVID-19. Se colectaron excretas de cacomixtles en 3 localidades con diferente grado de urbanización (entre 100 y 5% de vegetación natural) y las semillas fueron germinadas en cámaras de germinación. Se registraron 20 especies de plantas dispersadas, más que lo reportado en estudios previos. Más semillas fueron dispersadas en áreas naturales (7.1 semillas por g) que urbanizadas (3.2 semillas por g), pero la riqueza y diversidad fueron mayores en áreas urbanizadas. Ésto sugiere que la diversidad en ambientes urbanos es mayor, lo cual se puede atribuir a los microambientes formados por la infraestructura urbana y las plantas exóticas establecidas en el área.

Palabras clave: Endozoocoria; Ciudad de México; Opuntia; REPSA; Zoocoria

Introduction

Some animals may provide a key ecosystemic service, acting as seed dispersers, which allow many plant species to effectively move their offspring and maintain plant communities across different environments. An example of those animals is the ringtail (Procyonidae: Bassariscus astutus) which is an omnivorous and opportunistic animal that has shown potential to disperse the seeds of a great number of plant species across many ecosystems (Alexander et al., 1994; Rodríguez-Estrella et al., 2000; Rubalcava-Castillo et al., 2020). However, this important service could be diminished in urban ecosystems, where ringtails are very common (Barja & List, 2006; Swanson et al., 2022). Because urban areas offer new sources of food like anthropogenic waste and a variety of exotic plants, ringtails could disperse fewer seeds or seeds of exotic plants. This is an important concern since urban ecosystems are growing fast and thus becoming important areas for the conservation of species and areas on which we rely to obtain ecosystemic services.

Previous studies suggest that seed dispersal is diminished in cities due to a great number of unsuitable habitats (Cheptou et al., 2008) and barriers that obstruct animal movement and thus seed dispersal (Niu et al., 2018). However, animal-plant networks are persistent in cities (Cruz et al., 2013), and plants that rely on animal dispersal tend to have a more successful regeneration of populations than plants that rely on other strategies for dispersal (Niu et al., 2023). At the same time, most studies show that urban ecosystems tend to be more diverse than natural areas due to the great number of exotic species, microenvironments that can host greater plant diversity, and the fact that cities tend to be built in highly diverse locations (Kühn et al., 2004; Wania et al., 2006). Yet all these studies are performed in urban areas with both human activity and urban infrastructure; therefore, the hypothesis that urban areas are diverse due to the exotic plants and microhabitats and not due to “direct-human” seed dispersal (for example, seeds we throw away as garbage) is yet to be proven.

Particularly for the ringtails, Cisneros-Moreno and Martínez-Coronel (2019) found differences in the urban and rural ringtail diets. They report that in urban environments, ringtails consume 11 plant species, and 9 in rural environments. Other studies also show that ringtails commonly consume human-generated waste from trash cans when it is available (Castellanos et al., 2009; Picazo & García-Collazo, 2019). However, all those studies were made under normal human activity, but if it is reduced, the generation of waste could be diminished, affecting the ringtail diet, which in turn could lead to a change in their role as seed dispersers.

Therefore, this article aims to compare the diversity, abundance, and species of seeds dispersed by ringtails in 3 areas with different levels of urbanization during a time of reduced human activity due to the COVID-19 pandemic.

Materials and methods

This study was performed inside the main campus of the Universidad Nacional Autónoma de Mexico, located in Mexico City, Mexico. The campus contains a well-preserved ecological reserve (Reserva Ecológica del Pedregal de San Ángel; henceforth REPSA) and urban areas such as buildings and roads, all of which are surrounded by the Mexico City (Fig. 1). Therefore, a gradient between urban and natural areas can be found in a relatively small area (730 ha; Zambrano et al., 2016) that otherwise shares all environmental characteristics like mean temperature (18.2°C), precipitation (752 mm), original substrate, and vegetation: xerophitic shrubs (Rzedowski, 1954; SMN, 2023).

An important characteristic of this study is that it was performed under lockdown conditions due to the COVID-19 pandemic. Because of the rapid spreading of the virus, most activities on campus were switched to virtual mode; students took lessons from home; maintenance such as cleaning, gardening, and security were kept to a bare minimum; and all research activities had to be done from home, except for some specific cases, such as this study, that required special permission from the university. Those measures were implemented in March 2020 and began to be gradually lifted in the spring of 2022. Under normal conditions, the campus is visited by 166,474 people, and 70,000 vehicles, and 15 tons of waste (excluding gardening products) are generated (Zambrano et al., 2016). However, as a result of the pandemic, human activity on campus such as driving, waste generation and gardening, among others was minimal for 2 years. This gave us the opportunity to study the ringtail seed dispersal in an urban environment without human presence.

The correct identification of ringtail feces is an essential part of this project, since, in our study site, they could be confused with excretes of opossums (Didelphis virginiana). Previous studies suggest that opossums do not use latrines (Aranda, 2000), however, to ensure that latrines are used exclusively by ringtails, we placed camera traps in front of 8 latrines, and animal interactions with those latrines were recorded.

Figure 1. Map of the study location. Blue dots, Faculty (most urbanized area) latrines; red dots, the Institute latrines (semi-urban area); and green dots, the West core (natural area). The lines represent the 178 m around the latrines in which the percentages of the different types of terrain were calculated.

Three areas separated by at least 800 m were chosen to represent the urban-natural gradient: natural, semi-urban, and urban (Fig. 1). The home ranges of this species in the location are small: between 3 and 9.9 ha (Castellanos & List, 2005); therefore, this separation should ensure independence between the treatments. The level of urbanization was based on the percentage of area covered by natural vegetation, altered vegetation, impermeable areas without buildings (mainly roads and parking lots), and buildings found in a 178 m area (Fig. 1, Table 1) around the sampling points (178 m is the radius of the maximum activity area reported for ringtails in this particular location; Castellanos & List, 2005). The natural area (henceforth the West core) is located inside the west core of the REPSA. Vegetation consists mainly of shrubs, and Opuntia cactus is quite common (Cano-Santana, 1994). The semi-urban area (henceforth Institutes) is located around the humanitarian institutes area and consists of a mosaic of spatially located buildings, parking lots, altered vegetation (grass and some cultivated trees, mostly without fruit) and remnants of natural vegetation that surround this area on all sides (Fig. 1, Flores-Morales, 2023). The urban area (henceforth Faculty) is located inside the faculty of sciences and is dominated by tightly packed buildings divided by impermeable areas and gardens. The vegetation is diverse and includes a small amount of native plants such as Opuntia, but mostly consists of grass and introduced trees some of which have fruits that could be consumed by ringtails (Mendoza-Hernández & Cano-Santana, 2009). During the lockdown, gardens were left mostly unattended, and some alimentary plants began to grow (for example, we encountered several tomato plants with ripe fruits). The natural vegetation is located mostly on the edges of this area (Fig. 1).

Table 1

Amount of terrain coverage in the sampling areas. Impermeable areas were considered all areas covered with concrete but without buildings, mainly roads and parking lots.

	Natural vegetation (%)	Altered vegetation (%)	Buildings (%)	Impermeable areas (%)	Total area (ha)
West core	100	0	0	0	34.1 ha
Institutes	49.2	24.2	7	19.6	30.7 ha
Faculty	4.9	35	30.5	29.6	15.4 ha

To estimate the number of seeds dispersed by ringtails, we collected excretes from 13 latrines in each location, on January 18th 2022. Since previous studies report that seeds in our study area commonly have dormancy (Glebskiy, 2019), half of each latrine excretes was placed in plastic bags and half in mesh bags (with 1 × 1 mm openings). Both treatments were left in the field (on the soil and without cover) until April 29th 2022 (when the rains and thus the germination period started). The advantage of the plastic bag treatment is that it allows the seeds to experience the temperature changes that are responsible for ending dormancy in most plants and protects the seeds, but limits some other factors like gas exchange and humidity that could potentially contribute to the end of dormancy (Baskin & Baskin, 1998). On the other hand, the mesh bag allows for a better representation of the natural conditions to which seeds are exposed but is susceptible to losing seeds through the mesh and the addition of new seeds from the environment. Both methods were tested.

At the beginning of the rainy season (April 29^th 2022) bags were collected and put to germinate in commercial soil (the soil was sterilized by microwaving, and a control with no excretes was used to test the efficiency of sterilization and possible future seed additions) in a germination chamber (25°C, 16 hours of light, and 8 hours of darkness) for 4 months. All plant germinations were recorded and identified to morphospecies; when the plants grew, they were identified to the finest level possible. Species that germinated in the control pot were considered later additions and excluded from the analysis.

Data were analyzed with the R statistical packages: stats (R core team, 2022), dunn.test (Dinno, 2017), fossil (Vavrec, 2011), and vegan (Oksanen et al., 2022). Number of germinated seeds per gram of excrete was calculated. To compare between treatments (3 locations and 2 types of protection bags) Kruskal-Wallis and Dunn tests were performed for the total number of germinated seeds and the number of Opuntia seeds (this was the only species with enough data to analyze independently). A GLIM test (with Poisson distribution) was used to determine if the level of protection (plastic bags = 1, mesh bags = 0) and amount of vegetation (both natural and altered) influenced the amount of total and Opuntia germinated seeds. To compare the richness and diversity of dispersed seeds, we calculated the Shannon diversity and Chao 1 (± 95% confidence interval) richness. The similarity between treatments was measured using the Jaccard and Bray-Curtis indexes.

Results

A total effort of 329 trap nights was performed with 199 independent records (at least 1 hour between sightings) of ringtails, of which 44 times ringtails defecated in the latrine (Fig. 2). Opossums were observed 66 times, and no defecation was observed. At the same time, there were 9 observations of rodents and 7 of birds feeding from the latrines.

A total of 52 bags were recovered from the field (34 plastic, and 18 mesh bags), and were put to germinate. In total, 782 plants of 20 species (Table 2) germinated in this experiment. More seeds per gram of excrete germinated in the mesh bags treatment (U tests; V = 1,225, p < 0.001); however, more Opuntia seeds germinated in the plastic bag treatment (U test; V = 300, p < 0.001; Table 3). The Kruskal-Wallis test showed no differences in the number of germinated seeds between locations in the mesh bags, but there were significant differences for total seed and Opuntia seeds in the plastic bag treatment (p = 0.042 and p = 0.002). According to the Dunn test, there were fewer total seeds in the Faculty area than the West core (p = 0.009) and fewer Opuntia seeds in the Faculty area than the Institutes (p = 0.015) and the West core (p = 0.009).

GLIM analysis showed that both level of protection (-0.818, p < 0.001) and vegetation area (1.279, p < 0.001) are significant predictors for the number of total seeds germinated. For Opuntia seeds, protection (1.674, p < 0.001) and vegetation (3.559, p < 0.001).

Figure 2. a) Ringtail defecating in a latrine; b) a rodent consuming seeds from a latrine; c) a latrine; d) plants germinated from excretes.

We found significant differences in richness (according to Chao1) between the Faculty area and the West core (in plastic bags) and between the Faculty area and Institutes and the West core (in mesh bags; Table 4). The Bray-Curtis dendrogram shows 2 important groups: the mesh bag treatment and the plastic bag (Fig. 3). Jaccard index showed the following results within the same location,Faculty plastic-Faculty mesh: 0.714, Institutes plastic-Institutes mesh: 0.546, West core plastic-West core mesh: 0.571, total plastic-total mesh: 0.65; between locations,plastic bags, Faculty plastic-Institutes plastic: 0.769, Faculty plastic-West core plastic: 0.5, Institutes plastic-West core plastic: 0.643;between locations, mesh bags, Faculty mesh-Institutes mesh: 0.5, Faculty mesh-West core mesh: 0.294, Institutes mesh-West core mesh: 0.333.

Figure 3. Bray-Curtis dendrogram of germination treatments. First letter represents the location, W: west core, I: Institutes, F: Faculty; second letter, the type of bag: M: mesh, P: plastic.

Discussion

The camera trap experiment was designed to prove that the latrines from which we collected excretes belong to ringtails and not opossums since those animals produce very similar feces (Aranda, 2000). Given that we observed 44 events of defecation by ringtails and zero by opossums, it we can conclude that ringtails are the only latrine users. However, at the same time, rodents and birds were seen feeding in those latrines (Fig. 2). The ratio for those visits is 1 visit per 2.8 defecations, and this is important for seed dispersal, since most likely those visitors feed on seeds that are dropped by ringtails and can selectively remove some species. At the same time, it is interesting to consider the trade-off for the rodents that consume seeds from ringtail latrines since they are exposed to predation by the latrine owners. Although it is outside the scope of this research, we consider that the interaction around the latrines is a topic that should be further investigated to better understand the role of these animals as seed dispersers and the interactions that the latrines produce.

The comparison between plastic and mesh bags shows differences between the treatments, especially in the number of seeds that germinated per gram of excrete (Tables 2, 3). This could be attributed to the fact that mesh bags allow the smallest particles to exit the bag, and the total weight of feces diminishes while the number of seeds remains constant. Therefore, the mesh bag treatment is not adequate for estimating the number of seeds per gram of excrete, although data concerning the diversity and richness of seeds is still valid. Given the above and the fact that there were more plastic bag replicas, the data interpretation in this research is based on the plastic bag treatment.

Table 2

Number of seeds per gram of excrete in all treatments for each plant species.

Species	Common name	Faculty	Institutes	West core
Species	Common name	Plastic	Mesh	Plastic	Mesh	Plastic	Mesh
Ageratina sp. 1	Snakeroot	0.11	3.19	0.41	2.95	0.12	8.63
Ageratina sp. 2	Snakeroot	0.02	0.09	0.02	0	0	0
Asclepias linaria	Pineneedle milkweed	0	0	0	0	0.13	0
Amaranthaceae		0.33	0.19	0	0	0	0
Bidens sp.	Beggarticks	0	0	0.02	0	0.05	0.61
Cissus sicyoides	Princess vine	0	0	0	0	0.03	0.33
Conyza sp.	Horseweed	0.07	0.22	0.26	0	0	0
Drymaria laxiflora	Chickweed	0.04	0.27	0.12	0.35	0.03	2.68
Eragrostis sp.	Lovegrass	0	0.09	0	0	0	0
Iresine sp.	Bloodleaf	0	0	0	0	0	2.04
Opuntia sp.	Prickly pear	0.23	0.98	2.23	0.59	6.36	0.24
Solanaceae		0.03	0.27	0.08	0	0.1	0.71
Solanum nigrescens	Slender nightshade	0.1	2.79	0.04	2.14	0.08	0
Stevia sp.	Stevia	0	0.09	0	0	0	0
Phytolacca icosandra	Tropical pokeweed	0.46	0.15	0.25	0.22	0.08	0
Poaceae 1		0.02	0.39	0.12	0.07	0.13	0.17
Poaceae 2		0	0	0	0	0	0.25
Unknown sp. 1		0.02	0	0.1	0	0.05	0.33
Unknown sp. 2		0	0	0	0	0.05	0
Unknown sp. 3		1.72	0	0	0	0	0

Table 3.

Number of Opuntia and total seeds dispersed by ringtails in different environments. Values given in seeds per g of excrete ± S.D.

	Total seeds	Opuntia seeds
	Plastic	Mesh	Plastic	Mesh
West core	7.13 ± 8.06	15.99 ± 13.85	6.36 ± 7.58	0.24 ± 0.3
Institutes	3.64 ± 2.87	6.33 ± 6.61	2.23 ± 2.72	0.59 ± 1.33
Faculty	3.16 ± 7.09	8.72 ± 5.51	0.23 ± 0.75	0.98 ± 2.39
Total	4.7 ± 6.64	10.88 ± 10.26	2.96 ± 5.46	0.58 ± 1.5

GLIM analysis shows a positive relation between the number of seeds dispersed by ringtails and vegetation cover. Therefore, ringtails disperse fewer seeds in urban areas (Table 3); however, diversity and richness tend to be higher in the Faculty, the most urbanized location (Table 4).

Table 4

Richness (Chao1 ± 95% confidence intervals) and diversity (Shannon) of seeds dispersed by ringtails.

	Faculty	Institutes	West core	Total
	Plastic	Mesh	Total	Plastic	Mesh	Total	Plastic	Mesh	Total	Plastic	Mesh	Total
Observed richness	12	12	14	11	6	11	12	10	14	16	17	20
Chao1	16 ± 2.65	14.67 ± 1.85	18.5 ± 3.9	15 ± 2.65	8 ± 1.87	17 ± 0	12.17 ± 0.34	10.25 ± 0.44	14.5 ± 0.73	16.25 ± 0.44	19.67 ± 1.85	24.5 ± 3.4
Shannon	1.45	1.839	1.889	1.273	1.434	1.466	0.564	1.758	1.122	1.403	2.041	1.779

This is consistent with most previous studies that show a greater diversity of seeds in urban settings (Kühn et al., 2004; Wania et al., 2005), and that ringtails consume more plant species in the cities (Cisneros-Moreno & Martínez-Coronel, 2019). At our location, ringtails disperse fewer seeds in urban areas, but their richness and diversity are higher. The novel contribution of this research is that it was performed in an urban area with very little human activity; therefore, the direct effect of human activities such as waste generation and gardening could not explain the differences between treatments. At the same time, all 3 locations share very similar climatic conditions and originally were the same ecosystem. This suggests that differences between treatments are not due to original conditions (although it has been proven in other locations; Kühn et al., 2004). The high diversity of seeds in urbanized areas can be attributed to the great variety of habitats found in an urban area and the exotic species that have already been established there.

Ringtails are common in urban areas, and Castellanos et al. (2009) suggest they prefer disturbed areas over natural ones. This could be due to food availability in urbanized areas, and previous studies show that ringtails have a greater variety of food in urban areas. For example, Cisneros-Moreno and Martínez-Coronel (2019) show that an urban population consumes 36 food items and a rural population registered 28 items. Another advantage that cities offer is infrastructure. Poglayen-Neuwall and Toweill (1988) mention that rocky habitats favor ringtails, and human-made buildings provide a similar habitat. Interestingly, some data suggests that in the absence of humans, sightings of those animals in urban areas increased (Tzintzun-Sánchez, 2022; pers. obs.). This suggests that the benefits ringtails obtain from cities don’t come directly from human activities since, even without our presence, those animals have the benefits of infrastructure and a more diverse diet. However, further studies are needed to fully prove this hypothesis.

Previous studies have reported that fruits are important in the diet of B. astutus; however, the number of different plant species is generally low (13, ~ 9, 10, Alexander et al. [1994], Harrison [2012], and Rodríguez-Estrella et al. [2000], accordingly). In this study, 20 species of seeds were found and it is noteworthy that the cited articles included all vegetal matter in their analysis while this study only considers seeds that germinated. This suggests that the diversity of plants that are consumed in our site is much higher than usual. This could be the result of higher plant diversity in the location, or that ringtails tend to have a more frugivore diet here, this last hypothesis is supported by personal observations of the authors.

Based on the above, it could be concluded that there are several animals that consume the latrine contents, and this interaction could be important for seed dispersal. Ringtails disperse more seeds in natural areas, but their richness is higher in urban areas even in the absence of human activity.

Acknowledgements

We are thankful to M. E. Muñiz-Díaz for facilitating the germination chambers and her advice during this research, to Y. Martínez-Orea for helping with plant identification, to I. Castellanos-Vargas for technical support, and to the SEREPSA working team for facilitating the permission to perform this research. This project was financially supported by PAPIIT grant IN212121 (“El efecto de la urbanización sobre el tlacuache Didelphis virginiana en un matorral xerófilo de la Ciudad de México”), awarded to ZCS.

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ecología-junio2024

Perfil de leucocitos como biomarcador hematológicoen poblaciones de la salamandra de arroyo Ambystoma ordinarium

Carolina González-Pardo a, Ireri Suazo-Ortuño a, *, Cinthya Mendoza-Almeralla b, David Tafolla-Venegas c, Yurixhi Maldonado-López a y Esperanza Meléndez-Herrera a

Resumen

Leukocyte profile as hematologic biomarker in populations of the mountain salamander, Ambystoma ordinarium

Abstract

Ephemeral and intermittent xeroriparian systems arekeystone habitats for bird communities during thenon-breeding season in a Mexican semiarid landscape

Mónica E. Riojas-López a, Eric Mellink b, *, Moisés Montes-Olivares b

Abstract

Los sistemas xeroribereños efímeros e intermitentes son hábitats clave para comunidades de aves en la temporada no reproductiva en un paisaje semiárido mexicano

Resumen

Don’t count your eggs before they hatch: differential survival of artificial bird nests in an anthropogenically modified landscape in western Mexico

Dallas R. Levey a, b, Ian MacGregor-Fors c, *

Abstract

No cuentes los huevos antes de que eclosionen: supervivencia diferencial de nidos artificiales de aves en un paisaje antropogénicamente modificado en el oeste de México

Resumen

Ringtails (Bassariscus astutus) as seed dispersers in an urban gradient under conditions of low human activity due to COVID-19

Joselin Judith Peña-Herrera a, Yury Glebskiy a, b, *, Teresa de Jesús Hernández-Trejo a, Zenón Cano-Santana a

Abstract

Cacomixtles (Bassariscus astutus) como dispersores de semillas en un gradiente urbano bajo condiciones de baja actividad humana por COVID-19

Resumen

Carolina González-Pardo ^a, Ireri Suazo-Ortuño ^a,*, Cinthya Mendoza-Almeralla ^b, David Tafolla-Venegas ^c, Yurixhi Maldonado-López ^a y Esperanza Meléndez-Herrera ^a

Mónica E. Riojas-López ^a, Eric Mellink ^b,*, Moisés Montes-Olivares ^b

Dallas R. Levey ^{a, b}, Ian MacGregor-Fors ^c,*

Joselin Judith Peña-Herrera ^a, Yury Glebskiy ^{a, b,} *, Teresa de Jesús Hernández-Trejo ^a, Zenón Cano-Santana ^a