UNIVERSIDAD DE COSTA RICA 

SISTEMA DE ESTUDIOS DE POSGRADO 

 

 

 

 

EFECTOS DE LA CONTAMINACIÓN ANTROPOGÉNICA SOBRE LA 

COMUNICACIÓN ACÚSTICA DE ANFIBIOS EN AMBIENTES URBANOS 

 

 

 

 

Tesis sometida a la consideración de la Comisión del Programa de Estudios de Posgrado en 

Biología para optar por el grado de Maestría Académica en Biología 

 

 

 

ANA CECILIA GUTIÉRREZ VANNUCCHI 

 

 

 

Ciudad Universitaria Rodrigo Facio, Costa Rica 

2022



 
 

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Dedicatoria 

A Dios y a mi familia, quienes siempre han estado a mi lado y son mi más grande apoyo. 

Agradecimientos 

A Dios y a mi familia, por apoyarme e impulsarme durante todo el proceso, por siempre 

sostenerme, recordarme mis capacidades y darme la oportunidad de hacer lo que amo. A 

mis padres Edith Vannucchi y Milton Gutiérrez, sin quienes nada de esto hubiese sido 

posible, gracias por estar a mi lado en cada paso de mi formación, y a mis hermanas por 

continuamente hacerme preguntas sobre ciencia y naturaleza, aunque muchas veces yo no 

supiera la respuesta. 

A mis amigas Catalina, Ximena y Gloriana, por nunca soltarme la mano y ser una red de 

seguridad en los momentos más retadores. Gracias por ser un ejemplo de perseverancia, 

esfuerzo y disciplina. 

A Ferli por compartir tantos años de universidad juntos y hacer este proceso aún más 

enriquecedor, les estaré siempre agradecida por toda su compañía y apoyo. Mi paso por 

biología no sería lo mismo sin ustedes. 

Al Laboratorio de Ecología Urbana y Comunicación Animal por facilitarme todas las 

herramientas y materiales necesarios para realizar este proyecto, y a sus integrantes por su 

tiempo y retroalimentación. A Luis Sandoval, Raúl Bartolo y a mi mamá Edith Vannucchi, 

por toda su ayuda con los muestreos, grabaciones de ranas y acompañarme al campo,  y a 

Mónica Castro por su enorme ayuda con los análisis de cantos. Todos fueron parte 

invaluable de este proyecto,  sin ustedes hubiese sido todo mucho más complicado. 

A mi increíble comité de tesis, Luis Sandoval, Branko Hilje y Sofía Rodríguez, por toda su 

paciencia, consejos, comentarios, discusiones y por creer en este proyecto. Gracias por 

todo el conocimiento que compartieron conmigo durante estos años, no son solo grandes 

científicos, sino también grandes personas. 

Y por último pero no menos importante, a la Universidad de Costa Rica, a la Escuela de 

Biología y al Sistema de Estudios de Posgrado, por darme la oportunidad de tener una 

formación de calidad, aprendizajes, recuerdos y personas para toda la vida. 



 
 

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Índice general 

Contenido                                                                                                                      Página 

Dedicatoria y agradecimientos…………………………………………………………….. ii 

Hoja de aprobación………..……………………………………………………………… iii 

Resumen…..……………………………………………………………………………….. 1 

Índice de cuadros…………………………………………………………………………... 3 

Índice de figuras…………….……………………………………………………………... 4 

Introducción………………………………………………………………………………... 6 

 Contaminación acústica……………………………………………………………. 7 

 Contaminación lumínica………………………………………………………….... 9 

 Especie de estudio………………………………………………………………... 10 

Capítulo 1. Occurrences and effects of urbanization on amphibians: a review…………. 13 

 Abstract…………………………………………………………………………… 14 

 Introduction………………………………………………………………………. 14 

 Methods……………………………………………………………………........... 16 

  Literature search………………………………………………………….. 16 

  Data collection and analysis……………………………………………… 17 

 Results……………………………………………………………………………. 19 

 Discussion………………………………………………………………………… 20 

  Region differences in study publications………………………………… 20 

  Species classification and urban effects………………………………….. 20 

  Future directions of urban amphibian studies………………………......... 25 

References………………………………………………………………………... 25 



 
 

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Tables and Figures………………………………………………………………... 32 

Appendix 1……………………………………………………………………….. 38 

Capítulo 2. Effects of anthropogenic noise on the acoustic characteristics of a glass frog 

call in urban conditions…………………………………………………………………... 49 

Abstract…………………………………………………………………………… 50 

 Introduction…………………………………………………………………......... 50 

 Methods……………………………………………………………………........... 53 

  Study sites………………………………………………………………… 53 

  Recording and noise level measurements………………………………… 53 

  Recording analysis…………………………………………………........... 54 

  Statistical analysis………………………………………………………… 55 

 Results……………………………………………………………………………. 55 

  Effects of chronic anthropogenic noise on male advertisement calls…….. 55 

  Effects of instantaneous anthropogenic noise……………………………. 56 

 Discussion………………………………………………………………………… 56 

References………………………………………………………………………... 59 

Tables and Figures………………………………………………………………... 64 

Capítulo 3. Effects of light pollution and noise on the vocal activity of a glass frog in 

urban conditions………………………………………………………………………….. 68 

Abstract…………………………………………………………………………… 69 

 Introduction………………………………………………………………………. 69 

 Methods……………………………………………………………………........... 72 

  Light measurements and recordings……………………………………… 72 

  Recording analysis…………………….………………………………….. 73 



 
 

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  Statistical analysis………………………………………………………… 74 

 Results……………………………………………………………………………. 74 

 Discussion………………………………………………………………………… 75 

References………………………………………………………………………... 78 

Tables and Figures………………………………………………………………... 84 

Appendix 1……………………………………………………………………….. 89 

Conclusiones……………………………………………………………………………... 90 

Bibliografía……………………………………………………………………………….. 92



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Resumen 

El proceso de urbanización que se da de manera creciente a nivel mundial, conlleva 

cambios en el ambiente, entre los cuales se encuentra la aparición de contaminantes de 

origen antropogénico, en zonas donde antes no existían. Entre estos contaminantes se 

encuentran el ruido antropogénico y la contaminación lumínica, provocada por luces de 

origen artificial. Estos contaminantes pueden afectar distintos procesos en diferentes 

grupos de animales, entre los que se encuentra la comunicación acústica. 

La comunicación acústica es el principal método de comunicación en anuros, sin embargo, 

los efectos de la urbanización y más específicamente de la contaminación lumínica y el 

ruido antropogénico han sido menos estudiados en este grupo, que en otros grupos de 

animales como aves y mamíferos. Debido a esto, el conocimiento que tenemos sobre cómo 

los contaminantes antropogénicos pueden estar afectando la superviviencia de anuros en 

zonas urbanas, especialmente a largo plazo, es aún limitado. 

Nuestro objetivo con esta investigación fue determinar los efectos de la contaminación 

antropogénica en la comunicación acústica de anfibios presentes en ambientes urbanos. 

Más específicamente, queríamos determinar los efectos del ruido antropogénico y la 

contaminación lumínica sobre las características acústicas de las vocalizaciones de la rana 

de vidrio Hyalinobatrachium fleischmanni y sobre su actividad vocal. Esta especie de rana 

vive y se reproduce en quebradas pequeñas en ambientes urbanos, donde vocaliza desde las 

hojas, y está presente en sitios con distintos niveles de desarrollo urbano, con distintos 

niveles de intensidad lumínica y ruido. Además, el rango de frecuencia del canto de esta 

especie, traslapa en su parte baja con las frecuencias de ruido antropogénico, lo cual podría 

dificultar su comunicación acústica en ambientes con altos niveles de ruido. 

Realizamos una revisión bibliográfica de literatura científica a nivel global, para 

determinar el estado de conocimiento sobre anfibios en ambientes urbanos. Y obtuvimos la 

locación geográfica de los estudios, clasificamos las especies como “N/A” (cuando no 

teníamos suficiente información para clasificarlas),“explotadoras”, “sobrevivientes” y 

“evitadoras”, y los efectos de la urbanizaicón como “positivos”, “neutros” y “negativos”. 

Encontramos que la mayor cantidad de estudios pertenecieron al norte global, y fueron en 

su mayoría realizados en Estados Unidos. El mayor porcentaje de especies fue 

categorizada como N/A, seguido por especies evitadoras. Además, el mayor porcentaje de 

estudios indicó efectos negativos, lo cuales fueron reportados principalmente para las 



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especies evitadoras. El efecto negativo más reportado fue baja abundancia y/o ocurrencia 

de especies, y el efecto positivo más reportado fue alta abundancia y/o ocurrencia.  

Para investigar los efectos del ruido antropogénico en las características acústicas del canto 

de H. fleischmanni, trabajamos en dos sitios con distinto grado de desarrollo urbano. 

Grabamos 56 machos y medimos 7 caracterísiticas acústicas para el canto de cada macho y 

las relacionamos con el nivel de ruido antropogénico en ambos sitios. Encontramos que la 

duración del canto y el tiempo entre cantos fueron mayores en el sitio urbano, el cual tenía 

un nivel de ruido crónico mayor, y que la duración de la llamada y el tiempo entre 

llamadas disminuyó conforme aumentó el nivel de ruido crónico. La frecuencia mínima y 

la frecuencia de máxima amplitud también fueron mayores en el sitio con mayor nivel de 

ruido crónico. En cuanto al ruido instantaneousáneo, encontramos que el tiempo entre 

llamadas disminuyó con el aumento del ruido instantaneousáneo, pero el resto de las 

características acústicas no variaron. Es decir, el ruido crónico e instantaneousáneo, afectan 

de manera distinta las características acústicas del canto de H. fleischmanni. 

Para determinar los efectos de la contaminación lumínica y el ruido en la actividad vocal 

de H. fleischmanni, trabajamos en dos sitios con diferente grado de urbanización, ruido y 

abundancia de luces artíficiales. Medimos la intensidad lumínica y el ruido de fondo en 

cada punto de muestreo dentro de cada sitio de estudio, y dividimos los puntos de muestreo 

entre “iluminados” y “oscuros”, dependiendo de la cantidad de luz artificial en cada uno. 

Grabamos la actividad vocal de H. fleischmanni de las 16:00 a las 6:00 h en cada sitio de 

muestreo y obtuvimos una proporción de cantos por hora. El pico de actividad de la 

especie de estudio fue entre las 19:00 h y las 22:00 h. Al relacionar la proporción de cantos 

con los niveles de contaminación lumínica y ruido de fondo, encontramos que el ruido de 

fondo afectó los patrones de actividad vocal de manera distinta dependiendo de la hora, sin 

embargo, no encontramos un efecto de la contaminación lumínica sobre los patrones de 

actividad vocal de H. fleischmanni. 

 

 

 

 

 



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Índice de cuadros 

 

Capítulo 2. 

Table 1. Acoustic characteristics of Fleischmann’s Glass Frog calls, in two sites with 

different levels of urbanization. Values are average ± SD.………………………………. 65 

Capítulo 3. 

Table 1. Summary of the results for generalized linear mixed models with zero-inflated and 

Gaussian distribution, used to test if the proportion of calls changed according to different 

variables and their 

interactions…..…………………………………………………………………………… 84 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 



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Índice de figuras 

Introducción. 

Figura 1. Mapa de Costa Rica con el Gran Área Metropolitana señalada en rojo. Tomado 

del Plan de Ordenamiento Territorial de la Gran Área Metropolitana 2011-2030 (Rosales, 

2012)……………………………………………………………………………………… 12 

Capítulo 1.  

Figure 1. Percentage of urban effect studies on amphibians per country or region until 

November 2020 (n =104)…...……………………………………………………………. 32 

Figure 2. Percentage of urban effect studies per geographic region until November 2020 (n 

= 104)......…..…………………………………………………………………………….. 33 

Figure 3. Percentage of studies including amphibians in urban areas, per effect category of 

urbanization on amphibian species. Percentages add up more than 100% because some 

studies reported more than one effect in the same publication, for example, a positive effect 

for one species but a negative effect for other species….………………………………... 34 

Figure 4. Number of studies with negative, neutral and positive effects for each species 

category…………………………………………………………………………………... 35 

Figure 5. Number of studies on each negative effect category, per species category (i.e. 

avoiders, survivors, exploiters, and N/A)..………………………………………………. 36 

Figure 6. Number of studies on each negative effect category, per species category (i.e. 

avoiders, survivors, exploiters, and N/A)..………………………………………………. 37 

Capítulo 2. 

Figure 1. A. Map of Costa Rica with the two study sites marked with blue dots, and the 

square marking the Gran Área Metropolitana, where the study sites are located. B. Yellow 

dots mark the two study sites, the yellow dot on the bottom marks the urban study site, and 

the yellow dot on the top marks the rural study site. C. Urban study site with a creek 

marked in blue. The course of this creek was followed to put the automated recorders. D. 

Rural site with the creek followed to put the automated recorders marked in blue……… 64 



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Figure 2. Relationship between seven acoustic characteristics of Fleischmann’s Glass Frog 

male calls, and the chronic anthropogenic noise level (dB)……………………………… 66 

Figure 3. Relationship between the time between calls in Fleischmann’s Glass Frog male 

calls and the instantaneous anthropogenic noise level (dB)……………………………… 67 

Capítulo 3. 

Figure 1. Light intensity measurement points within each light and dark sampling point. 

The star at the center marks the location of the recorder and one light intensity 

measurement point. The red dots mark four light intensity measurement points taken 2 m 

apart from the recorder and at 90° from each other……………………………………… 85 

Figure 2. Figure shows average levels of light intensity (lux) and background noise level 

(dB -1) between sites with lower and higher levels of urbanization in our study (first line), 

between light and dark sites in our study (second line), and for the interaction of light 

intensity and study site (third line on the left), and the interaction of background noise and 

study site (third line on the right)………………………………………………………… 86 

Figure 3. Proportion of Fleischmann’s Glass Frog calls per hours of the day. The dots 

represent the mean call proportion per each recorded hour including all sampling points in 

the study, with their standard deviation represented by the lines………………………… 87 

Figure 4. Proportion of calls in relation to the background noise level (dB) for each 

recorded hour from 16:00 h to 6:00 h. Each square shows the call proportion distribution 

according to the background noise level (dB) for each of the 14 recorded hours 

separately…………………………………………………………………………………. 88 

   

 

 

 

 

 

 

 



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INTRODUCCIÓN 

El proceso de urbanización es un fenómeno creciente a nivel mundial que conlleva la 

expansión de zonas urbanas hacia zonas rurales, y la de estas hacia zonas naturales (Joyce, 

2006). Este proceso se asocia a un acelerado crecimiento poblacional en escala global, 

durante las últimas tres décadas (Stein et al., 2000; McKinney, 2002; Estado de la Nación, 

2018). En Costa Rica el crecimiento urbano ha sido incentivado por las políticas 

económicas y sociales, causando una rápida expansión horizontal del Gran Área 

Metropolitana (GAM; Limitada al este por Ochomogo, al oeste por San Ramón y Atenas, 

al norte por la Cordillera Volcánica Central y al sur por los Cerros de Escazú) (Fig.1) 

(Estado de la Nación, 2018). Esto ha provocado la eliminación de plantaciones (de café, 

caña o pasto), zonas de crecimiento secundario, o remanentes de bosques, para la 

construcción de viviendas y comercios (Joyce, 2006; Pauchard et al., 2006; Estado de la 

Nación, 2018).  

El aumento de la urbanización produce un incremento en la contaminación sónica, 

lumínica, del aire y los suelos, aumenta la temperatura, la compactación de suelos y acelera 

la pérdida de los parches de vegetación natural (Medley et al., 1995; Pickett et al., 2001; 

McKinney, 2002). Estos cambios en la estructura del ambiente causan una disminución o 

desplazamiento de la mayoría de las especies nativas de la zona, debido al cambio de las 

condiciones ambientales necesarias para su supervivencia (Marzluff, 2001; McKinney, 

2002; Biamonte et al., 2011). Este desplazamiento de especies nativas genera un aumento 

en un número pequeño de especies colonizadoras que contribuye a la homogenización de 

la diversidad en sitios urbanos (Blair, 2001).  

Con los cambios en el ambiente producto de la urbanización aparecen tres clasificaciones 

para los animales, que dependen de su respuesta a estos cambios. Existen 1) las especies  

“evitadoras”, que se alejan del centro urbano y se mantienen en el interior de los bosques, 

2) las especies “adaptadoras” que usualmente tienen cierto grado de tolerancia a los 

cambios por urbanización, y que normalmente se encuentran en las periferias de los centros 

urbanos y por último 3) las especies “explotadoras”, las cuales suelen ser comensales y 

toman provecho de los recursos que la urbanización les presenta, como fuentes estables de 

alimento y agua de origen antropogénico; este último grupo de especies ha sido capaz de 

adaptarse y sobrevivir bajo estas condiciones. (McKinney, 2002). Algunos ejemplos de 

especies “evitadoras” son las aves Crypturellus soui y Myadestes melanops (Biamonte et 



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al., 2011), lagartijas como Uta stansburiana  y Phrynosoma solare (Germaine & 

Wakeling, 2001) y algunos mamíferos como el zorro rojo (Vulpes vulpes) (Randa & 

Yunger, 2006). En cuanto a ejemplos de especies “adaptadoras” se encuentran algunos 

anfibios como el sapo Alytes obstetricans y las ranas Pelophylax ridibundus y aves como la 

lechuza Strix aluco y la garza Ardea cinerea (Laurian, 2012). Por último existen varios 

ejemplos comunes de especies “explotadoras” como  las palomas comunes (Columba livia) 

y los zanates (Quiscalus mexicanus), los mapaches (Procyon lotor) y ratas (Rattus rattus) y 

anfibios como la rana coquí (Eleutherodactylus coqui), que alcanzan densidades mucho 

mayores en zonas urbanizadas que en zonas naturales (Woolbright et al., 2006).  

Los estudios de especies que han logrado adaptarse a zonas urbanas son limitados y la 

mayoría están representados por reportes de aves (Blair, 2001; Marzluff, 2001; Biamonte 

et al., 2011) y de riqueza de especies en ambientes urbanos versus ambientes rurales para 

mamíferos, lagartijas y algunos insectos (Mackin-Roglaska et al., 1988; Germaine & 

Wakeling, 2000; McIntyre, 2000; Pawlikowski & Polorniecka, 1990; Nuhn & Wright, 

1979). Para anfibios, existe aún menos información sobre las especies que han logrado 

adaptarse a estos cambios en el ambiente y los efectos que la urbanización ha tenido sobre 

el grupo en general (compilado en Mitchell et al., 2008). Dado el acelerado crecimiento del 

proceso de urbanización, es de vital importancia tener conocimiento sobre la ecología de 

diversos grupos, tanto en ambientes naturales como urbanos, para comprender las 

adaptaciones a nuevas fuentes de contaminación. Por ejemplo, la contaminación acústica 

por ruido antropogénico (motores, música) y la contaminación lumínica por la aparición de 

fuentes de luz artificial durante la noche, que pueden afectar la ecología de diferentes 

especies de animales.  

Contaminación acústica 

La comunicación acústica representa una de las formas de comunicación principal en 

muchos grupos de animales como aves, mamíferos, anfibios y reptiles (Ryan, 2001; 

Bradbury &Vehrencamp, 1998). Ya que es utilizada en las interacciones sociales como 

cortejo, copula, defensa de territorio, o encuentros agonísticos (McGregor, 2005; Brumm, 

2013; Vitt & Caldwell, 2013). Los sonidos utilizados en la comunicación acústica están 

determinados por múltiples parámetros o características espectro-temporales como lo son 

la energía del sonido en decibeles, la frecuencia en hertzio, la duración del sonido y la 

temporalidad (momento del día en que se realiza) (Bradbury & Vehrencamp, 1998). 



8 
 

 
 

Las características del ambiente (como ruido por viento y fuentes de agua, densidad de la 

vegetación y temperatura), influyen en la forma en que se comunican acústicamente los 

animales, como lo propone la Hipótesis de Adaptación Acústica (Morton, 1975; Hansen, 

1979). Una nueva característica del ambiente que puede afectar la comunicación acústica 

es el ruido antropogénico producto de los motores de los vehículos (ej. automóviles, trenes, 

aviones), motores de fábricas, el paso de personas, la música, y cualquier otra fuente de 

sonido producido por los humanos. El ruido antropogénico, contrario al ruido de origen 

natural (producido por ríos, viento, cantos de otras especies), es más constante en el 

tiempo, es de origen muy reciente (desde mediados del siglo XVIII con la revolución 

industrial), y ocurre en sitios que antes no poseían altos niveles de ruido (Kunc & Schmidt, 

2019). Lo anterior dificulta que muchas especies de animales puedan comunicarse por 

medio de vocalizaciones (señales acústicas) dentro de zonas urbanas, ya que las 

frecuencias de sus vocalizaciones traslapan con las frecuencias del ruido antropogénico 

(enmascaramiento de las señales acústicas) que ocurre por debajo de los 5kHz (Wood 

&Yezerinac, 2006; Hanna et al., 2014).    

Se ha encontrado que algunos grupos de animales tienen la capacidad de modificar las 

características espectro-temporales de sus vocalizaciones para evitar el enmascaramiento 

por ruido antropogénico (Slabbekoorn & Peet, 2003). Dentro de las estrategias que utilizan 

distintos grupos de animales para evitar el enmascaramiento acústico, está aumentar las 

frecuencias  de su canto para reducir o eliminar el traslape con el ruido, como sucede para 

varias especies de aves como Parus major (Slabbekoorn & Peet, 2003) y algunos anfibios 

como la rana Litoria ewingii (Parris et al., 2009). También pueden modificar los periodos 

de vocalización para evitar las horas con mayores niveles de ruido como ocurre en algunos 

mamíferos como el mono Callicebus nigrifrons (Duarte et al., 2018) o modificar su tasa de 

canto como el caso de las ranas Microhyla butleri y Rana taipehensis (Sun & Narins, 

2005). 

Esta variación de las características espectro-temporales del canto o periodos de 

vocalización, se conoce como plasticidad acústica y esta a su vez puede variar entre 

poblaciones o entre individuos de una misma población (Cunnington & Farig, 2010). La 

plasticidad acústica permite a las especies minimizar los efectos de enmascaramiento por 

ruido antropogénico. Sin embargo, se sabe que modificar la intensidad y frecuencia del 

canto, vocalizar una mayor cantidad de horas, o cantar a horas distintas de las horas 

usuales de actividad implica un gasto de energía mayor para algunos individuos (Brumm, 



9 
 

 
 

2013).  El efecto del ruido en las vocalizaciones de anuros ha sido poco estudiado en 

comparación con otros grupos de animales y los estudios han tenido resultados diversos en 

cuanto a modificación de las vocalizaciones en este grupo (Sun & Narins, 2005; Bee & 

Swanson, 2007; Lengagne, 2008; Herrera-Montes & Aide, 2011 ). De modo que las 

estrategias que utilizan los anfibios,  para evitar el enmascaramiento acústico por ruido 

antropogénico y las implicaciones que esto tiene en la plasticidad de sus vocalizaciones 

aún son poco conocidas.  

Contaminación lumínica 

La urbanización aumenta la cantidad de fuentes de luz no naturales durante las noches. 

Este tipo de iluminación está constituida por cualquier fuente de luz de origen 

antropogénico -las luces de las calles, estadios, casas, carros, anuncios- (Perry et al., 2008), 

tiende a ser mucho más brillante que la luz natural y afectan todas las áreas urbanas 

(Cinzano et al., 2001; Bennie et al., 2015). Esto genera en dichas áreas contaminación 

lumínica, definida como un exceso de luz proveniente de fuentes antropogénicas. 

Adicionalmente, el brillo de estas luces se refleja en las nubes causando una iluminación 

nocturna mayor a la natural, especialmente en las áreas adyacentes a los centros urbanos 

(Cinzano et al., 2001). En consecuencia los efectos de la contaminación lumínica se 

expanden más allá de los sitios donde están presentes las fuentes de luz artificial.  

 A pesar del gran alcance que puede llegar a tener la contaminación lumínica, sus 

efectos sobre la fauna y el ambiente en general han sido mucho menos estudiados que los 

de otros tipos de contaminación de origen antropogénico como la contaminación por 

sólidos, la contaminación acústica, o la química  (Longcore & Rich, 2004; Perry et al., 

2008). La mayoría de los estudios sobre contaminación lumínica, ha estudiado su efecto en  

aves, siendo el resultado principal el cambio en los patrones temporales de actividad 

acústica en aves diurnas (Miller, 2006; Da Silva et al., 2015). Al haber un exceso de luz 

durante la noche, las aves extiendan sus horas de actividad aumentando las horas de 

vocalizaciones en el día, y por ende reduciendo el tiempo de descanso (Byrkjedal et al., 

2012; Raap et al., 2015). En peces como salmones se ha encontrado que la luz artificial 

causa una detección mayor de presas y altera el tiempo de migración nocturna (Metcalfe et 

al., 1997; Riley et al., 2012). En mamíferos, como algunos roedores nocturnos, se han 

encontrado cambios en su ciclo circadiano y una actividad nocturna reducida (Sharma et 

al., 1997; Kramer & Birney, 2001). Los estudios para medir el efecto de esta 



10 
 

 
 

contaminación en reptiles son escasos (Perry et al., 2008) y se centran básicamente en el 

análisis de la actividad de forrajeo y reportes de ocurrencias de especies cerca de centros 

con luz artificial (Case et al., 1994; Meshaka et al., 2004; Powell et al., 2005; Perry & 

Fisher, 2006). La excepción en este grupo son los estudios que han analizado los efectos 

adversos de la iluminación artificial en el comportamiento de desove de las tortugas 

marinas (Witherington & Martin, 2000; Tuxbury & Salmon, 2005; Bourgeois et al., 2009; 

Kamrowski et al., 2012), por ser importante para la conservación de las playas de 

anidación. 

Los anfibios tampoco son la excepción a la falta de información del efecto de la 

contaminación lumínica, pese a que son un grupo principalmente nocturno (Savage, 2002; 

Perry et al., 2008). La comunicación acústica en anuros (ranas y sapos) es de vital 

importancia para todas sus interacciones sociales, y por ende la temporalidad de su 

actividad acústica se vuelve también un factor determinante para la comunicación efectiva 

entre individuos (Schwartz & Bee, 2013; Vitt & Caldwell, 2013; Bevier, 2016; 

Colafrancesco & Gridi-Papp, 2016). Un aumento en el nivel de iluminación podría 

significar un cambio en las horas de actividad y en el comportamiento de varias especies 

(Meshaka et al., 2014, Henderson & Powell, 2001; Perry & Fisher, 2006). Los efectos que 

esto pueda tener sobre las relaciones entre individuos (ej.: atracción de pareja, defensa de 

territorio, o detección de depredadores) tanto a nivel intra- como inter-específico son aún 

desconocidos. Por lo tanto, estudiar el efecto de la contaminación lumínica sobre las 

especies de anuros que habitan áreas urbanas es necesario para generar medidas correctivas 

y de manejo que faciliten la conservación de estas especies. 

Especie de estudio 

A pesar de los efectos de la contaminación acústica y lumínica sobre la comunicación 

acústica, se conoce que hay especies de anfibios que sobreviven y se reproducen en 

ambientes urbanos como los anuros (Perry et al., 2008). La rana de vidrio 

Hyalinobatrachium fleischmanni vive y se reproduce dentro de pequeños ríos en ambientes 

urbanos, desde donde cantan sobre las hojas (Kubicki, 2007). El canto de esta especie 

presenta un rango de frecuencias entre 3.8 y los 5.3 kHz (Savage, 2002; Kubicki, 2007), 

traslapando así con las frecuencias del ruido antropogénico. Al ser una especie común en 

ambientes urbanos, puede ver afectada su comunicación acústica por los altos niveles de 

ruido o la iluminación intensa y constante presente en estos ambientes. Esta situación 



11 
 

 
 

puede provocar el enmascaramiento de sus señales acústicas, evitando que el mensaje sea 

transmitido al receptor de forma efectiva. Debido al traslape entre el canto y el ruido, y la 

presencia de iluminación artificial en ambientes urbanos, espero que H. fleischmanni 

modifique las características espectro-temporales de su canto y las horas de actividad 

acústica, para mejorar la eficiencia de su comunicación.  

 

 

 

 

 

 

 

 

 

 



12 
 

 
 

 

Figura 1. Mapa de Costa Rica con el Gran Área Metropolitana señalada en rojo. Tomado 

del Plan de Ordenamiento Territorial de la Gran Área Metropolitana 2011-2030 (Rosales, 

2012). 

 

 

 

 

 

 

 

 



13 
 

 
 

 

 

 

 

 

 

 

 

 

 

Capítulo 1. Occurrences and effects of urbanization on amphibians: a review 

 

 

 

 

 

 

 

 

 

 

 

 



14 
 

 
 

Abstract. Urbanization causes changes in natural landscapes. It causes a decrease or 

displacement of native species from urban areas, contributing to homogenization of 

diversity. Based on the response of a species to changes in the environment, they can be 

classified into urban “exploiters”, “survivors”, and “avoiders”. Because amphibians in 

urban areas have been less studied than other animal groups, our knowledge of the effects 

of urbanization on amphibians is limited. Our goal was to conduct a literature review about 

the occurrence of amphibians in urban areas, and the effects of urbanization on amphibians 

at a global scale, to identify information gaps and propose future research directions. We 

conducted a search of peer-reviewed scientific literature and from 104 selected studies; we 

extracted the geographical location, the effects of urbanization reported (positive, negative, 

neutral) and the species abundance/occurrence to classify them as exploiters, survivors or 

avoiders. The United States had the largest number of studies, and the majority of studies 

belonged to the Global North. The highest percentage of species was categorized as N/A 

followed by avoiders. The highest percentage of studies indicated negative effects, and 

those negative effects were mostly reported for avoider species. The most commonly 

reported negative effect was low abundance and/or occurrence, and the most commonly 

reported positive effect was high abundance and/or occurrence. Only a small group of 

species (exploiters) obtained benefits from urban sites, and the large majority of studies 

come from the Global North, where species richness is lower. This, along with a lack of 

long-term studies, can compromise our understanding of the effects of urbanization on 

amphibians. We recommend increasing the number of long-term studies in the Global 

South, making direct comparisons between urban and natural environments, and 

continuing to make species classifications regarding their response to urbanization, to 

better standardize future revisions.  

Key words: urban ecology, city, amphibians 

The process of urbanization is a growing phenomenon worldwide, which entails the 

expansion of urban areas towards rural areas, and the expansion of rural areas to natural 

areas (Joyce, 2006). It is associated with a rapid population growth worldwide, especially 

during the last three decades (Stein et al., 2000; McKinney, 2002; Estado de la Nación, 

2018). Currently, urban areas constitute approximately 4% of the earth’s surface and 

support more than 50% of the human population (Rosen, 2000; United Nations Department 

of Economic and Social Affairs, 2019). Urbanization encompasses the physical, 

anthropological, and economic processes that change natural landscapes to those 



15 
 

 
 

dominated by human activities (Mitchell & Brown, 2008). The increase in urbanization 

produces an increase in noise, light, air and soil pollution, temperature, soil compaction, 

and accelerates the loss of natural vegetation patches (Medley et al., 1995; Pickett et al., 

2001; McKinney, 2002) producing a decrease or displacement of native species of fauna 

from urban areas (Marzluff, 2001; McKinney, 2002; Biamonte et al., 2011). This 

displacement of native species generates an increase of colonizing species that contribute 

to the homogenization of diversity in urban areas (Blair, 2001). 

Based on how species respond to changes in the environment that are produced by 

urbanization, species are classified in three groups (McKinney, 2002).  "Avoider" species 

move away from the urban center and stay inside the forests. "Survivor" species usually 

have a certain degree of tolerance to changes caused by urbanization, and are normally 

found on the outskirts of urban centers. “Exploiter” species are usually commensals and 

take advantage of the resources offered by urbanization, such as stable sources of food and 

water of anthropogenic origin, and are able to adapt and survive under these urbanized new 

conditions, and might become dependent on urban resources (McKinney, 2002). Studies of 

species that adapt to urban areas are limited and are most represented by reports of birds 

(Blair, 2001; Marzluff, 2001; Biamonte et al., 2011), as well as studies of species richness 

in urban environments versus rural environments for mammals, lizards, and some insects 

(Mackin-Roglaska et al., 1988; Germaine & Wakeling, 2000; McIntyre, 2000; 

Pawlikowski & Polorniecka, 1990; Nuhn & Wright, 1979). Therefore, to understand which 

species are part of each group (“avoiders”, “survivors”, and “exploiters”), and how they 

respond to environmental changes, it is key to analyze the impact of urbanization on 

multiple animal groups and species. 

Amphibians have been less studied in urban areas relative to birds (e.g., Erz, 1966; 

Marzluff, 2001; Seress & Liker, 2015; Isaksson, 2018), plants (e.g., Pysek, 1989; King & 

Buckney, 2000; Chocholouskova & Pysek, 2003, Witting, 2004), and arthropods (e.g., 

McIntyre, 2000; Raupp et al., 2010; Bang & Faeth, 2011; Fenoglio et al., 2020). However, 

reports of amphibians in urban areas appeared as early as 1902, from the city of 

Washington, with a list of the batrachia and reptilia of the District of Columbia and vicinity 

(Hay, 1902), and in 1905, with a report of the batrachians in the vicinity of New York City 

(Ditmars, 1905; Mitchell & Brown, 2008). More recently, studies about the effect of 

urbanization on amphibians have focused on determining which species are present and 

can survive in urban areas (Entiauspe-Neto et al., 2016; Hill et al., 2017; Melo et al., 2018; 



16 
 

 
 

Ingle et al., 2019; Konowalik et al., 2020) and on the causes of population declines in cities 

(Martinez-Solano & García-Paris, 2001; Mollov, 2005; Price et al., 2006; Mitchell & 

Brown, 2008). But, information about other ecological processes (e.g., diet changes, 

mortality rate, or reproductive success), evolutionary responses (e.g., behavioral 

adaptation, or genetic and morphology changes), and changes in communication (e.g., 

changes in duration and frequency of calls) of amphibians in urban areas is still limited 

(Mitchell & Brown, 2008). Additionally, the majority of studies about amphibians in urban 

areas are from temperate regions (Mitchell, Brown & Barholomew, 2008). Given the rapid 

growth of urbanization, and very limited knowledge of its effect on amphibians, it is timely 

to generate a literature review to better understand how species are responding to 

urbanization. Therefore, our main goal was to conduct an exhaustive literature review 

about the ocurrence of amphibians in urban areas and the main effects of urbanization on 

this group. We also want to identify information gaps and propose future research 

directions to improve the knowledge of amphibian urban ecology and conservation. 

 

Methods 

Literature search 

We conducted a search of peer-reviewed scientific literature in November 2020 using 

Google Scholar (https://scholar.google.com/) and Web of Science databases 

(http://webofknowledge.com). Both databases were used to search for the following terms 

and their combinations: “Urban herpetofauna”, “Urban amphibians”, “cities” AND 

“herpetofauna”, “cities” AND “amphibians”, “cities” AND “frogs”, “cities” AND 

“salamanders”, “cities” AND “newts”, “cities” AND “caecilians”. 

For each search, we checked only the first 50 references that were generated, because after 

50, the references started to repeat between searches, or the results were not very relevant 

to the term searched. In addition, we reviewed the bibliography of all selected peer-

reviewed manuscripts in order to include other sources of information in the review. Also, 

we decided to exclude meta-analyses and previous reviews that included amphibians (n 

=43), because we preferred not to use previously analyzed data, and rather use the original 

source of information. Therefore, we considered the literature used in these reviews and 

https://scholar.google.com/
http://webofknowledge.com/


17 
 

 
 

meta-analyses, and included the references that met our choice criteria (see below), if they 

were not found previously under the search terms in both databases. 

Data collection and analysis 

We obtained 245 studies from the database search and 41 from reviewing the literature of 

the studies selected from the database, meta-analyses, and other reviews. To be included in 

the analysis, the studies needed to report the occurrence of amphibians in urban 

environments (presence, abundance, or comparison between urban or other habitats) or 

report the effects of urbanization on amphibian morphology, behavior, survival, diet, or 

evolution. We excluded studies that analyzed the effect of anthropogenic pollutants in 

laboratories or experimentally inside cities. We also excluded reports of amphibian deaths 

on roads, if roads were outside of cities (i.e., a road outside of a natural park or in the 

middle of a desert), or did not compare city roads versus rural, or natural roads or a 

gradient of road density as a measure for urbanization. After all these selection criteria, 104 

studies met the inclusion criteria and were used in this study (Appendix 1). 

From all selected studies, we extracted the geographical location of the reports, the effects 

of urbanization on amphibians when compared to natural or rural environments or reported 

by the authors (i.e., positive, negative, neutral), and its relative or quantitative abundance. 

We used the species abundance or occurrence in each study (when include in the study) to 

classify the species into three groups: exploiters, survivors, or avoiders. Species were 

classified as exploiters if there was a reported increase in population size or colonizing 

events when compared between rural or natural environments, when the population size or 

abundance was greater at urban sites compared to rural or natural sites, if the species were 

classified as “abundant”, “very common” or “common” by the authors, or if they had an 

occurrence percentage of 50% or more in the urban study sites. Species were classified as 

urban survivors if the population size was not larger in either rural or natural areas but 

species were still present in urbanized areas, if the population size was constant over time 

as long as it was not a species classified as “abundant”, “very common” or “common”, or 

if the occurrence percentage was between 15% and 49% in the study sites. Finally, species 

were classified as avoiders if the population size was very small or the species were not 

found in the more urbanized areas, if the species were classified as “uncommon” or “rare”, 

or if they had fewer than 15% of occurrence in the study sites. The criteria we used for the 

classification of amphibians and the effects of urbanization in this review were based on 



18 
 

 
 

and then adapted from the definitions of McKinney (2002). When the studies did not give 

enough information according to our criteria to put the species in one of the three 

aforementioned categories, we classified them as N/A.  

For the effect of urbanization on amphibian biology we classified it as positive when there 

was an increase in population size, a higher number of colonization events, the species was 

more common or abundant in urban areas than in natural areas or there was a more specific 

positive effect reported by the authors (increase in the individual size or lower mortality). 

We classified the effect as negative when the population size decreased due to urbanization 

or the species was only found in non-urban areas, or when there was a more specific 

negative effect reported by the authors (low genetic variability, mortality due to road 

collisions, tissue damage). When the effect could not be clearly classified as positive or 

negative, or when there was not enough information in the study to classify it in one of the 

aforementioned categories according to our criteria, we classified it as neutral. 

We calculated the percentage of each species category (exploiter, survivor, avoider, and 

N/A) per study, and then estimated the average for all studies. We also calculated the 

average number of species per category, in the studies that reported each category (average 

number of exploiter species in the studies that reported exploiter species). We calculated 

the percentage of studies for each effect category of urbanization on amphibians (positive, 

negative, or neutral), and the percentage of each effect category per amphibian category 

(exploiter, survivor, avoider, or N/A). We also calculated the percentage of studies per 

geographical location.  

Finally, we classified the negative and positive effects of urbanization into categories, to 

count which were the most common negative and positive effects reported in the literature. 

We classified the negative effects into: 1) Reduction or small population size, 2) Reduction 

or low genetic variability, 3) Low abundance and/or occurrence in urban spaces, 4) Lower 

species richness, 5) Local extinction of one or more species in a study site due to 

urbanization, 6) Mortality reports due to urbanization, 7) Negative reproductive effects, 

and 8) Physiological damage (tissue damage or negative hormonal effects). We classified 

the positive effects into: 1) Increase in or large population size, 2) High abundance and 

or/occurrence, 3) Higher species richness, 4) Colonization events, 5) Fewer diseases, and 

6) Positive effects on survival. Then, we counted the number of studies that reported 

positive or negative effects on each category, per species category (avoiders, survivors, 



19 
 

 
 

exploiters, and N/A). We did this in order to identify where the majority of information is 

generated (and therefore, where there is a lack of information) geographically, how the 

majority of amphibians are responding to urbanization (exploiters with positive effects or 

avoiders with negative effects), and what are the most commonly reported effects (whether 

positive or negative) for amphibians in urban environments. 

 

Results 

We found 104 studies that met inclusion criteria, which were conducted in 29 different 

countries or regions. The United States had the largest number of studies, representing 

37.5%, followed by Australia with 14.4%, and Brazil with 6.7%. The other 26 countries 

each accounted for less than 5% of the studies and 41.3% combined (Fig. 1). When we 

divided the studies into eight geographic regions (according to the Department of 

Homeland Security of the United States, https://www.dhs.gov/geographic-regions), North 

America accounted for the highest percentage of studies with 42.3%, followed by Europe 

with 25.0%, and Oceania with 14.4%. The other geographic regions accounted for less 

than 10% of the studies (Fig. 2). 

On average, the highest percentage of species in the studies were categorized as N/A 

(40.6% ± 47.2%), followed by avoiders (23.9% ± 32.5%), survivors (18.7% ± 30.1%), and 

the lowest percentage was classified as exploiters (16.8% ± 27.8%). For the studies in 

which species were classified as N/A, the average number of N/A species studied was 5.6 

± 6.5. For the studies that reported survivors, the average number of survivor species 

studied was 5.4 ± 6.8. For the studies that reported avoiders, the average number of avoider 

species studied was 4.5 ± 3.6; and for the studies that reported exploiters, the average 

number of exploiter species studied was 3.2 ± 1.6. 

Most studies indicated negative effects of urbanization on amphibians, followed by neutral 

effects, and then positive effects (Fig. 3). When we combined the species classifications 

and the effects classifications we found that for avoider species, the highest number of 

studies indicated negative effects. For the survivor species, the highest number of studies 

indicated neutral effects, followed by negative effects. For the exploiter species, the 

highest number of studies indicated positive effects, and for the N/A species, the highest 

number of studies indicated neutral and negative effects (Fig. 4).  



20 
 

 
 

The most commonly reported negative effect of urbanization for amphibians was low 

abundance and occurrence (n = 54), and it was mostly reported for avoider species (n = 

35), followed by lower richness (n = 13), and reduction of population size (n = 12), also 

mostly reported for avoider species (n = 5 and n = 4, respectively; Fig. 5). The most 

commonly reported positive effects of urbanization for amphibians were high abundance 

and/or occurrence (n = 22) mostly reported for exploiter species (n = 20), and colonization 

events (n = 3), and higher population size (n = 2), also mostly reported for exploiter 

species (n = 3 and n = 2, respectively; Fig. 6). 

 

Discussion 

Regional differences in study publications 

We found that most of the studies included in this review were conducted in North 

America, more specifically in the United States, followed by the European region and 

Australia, which means most of the studies were conducted and produced by the Global 

North. This might be because these are regions with high levels of urban development 

(United Nations Department of Economic and Social Affairs, 2019), as well as greater 

economic resources (as developed countries) compared to other areas of the world like 

Central America, South America, and Africa, where developing countries are located 

(United Nations Department for Economic and Social Affairs, 2020). This agrees with the 

findings of Karlsson et al. (2007), who found that most of the papers included in their 

review were published in the Global North or temperate/cold regions (around 80%), while 

the least number of studies were published from and about the Global South or sub-

tropical/tropical regions (around 13%). Several authors have also demonstrated that the 

number of scientific contributions are related to the economic resource of countries 

(Rodriguez-Navarro & Brito, 2022; Allik et al., 2020; Cimini et al., 2014), which is also 

supported by our results.  

Species classification and urban effects 

Many studies did not provide enough information, according to our criteria, to classify the 

species into avoiders, survivors or exploiters, but when we were able to classify the species 

into these categories, the majority of reports were of avoider species, and the minority of 

exploiter species. The studies that reported exploiter species had, on average, a lower 



21 
 

 
 

number of species per study than the studies that reported avoider and survivor species. 

This indicates that, according to our criteria, most of the amphibian species included in 

urbanization studies were avoiders, and the least were exploiters. Our results support 

Blair´s (2001) idea about diversity homogenization in cities, because there is evidence for a 

lower number of species that are able to adapt to the urbanization process, live, and 

reproduce successfully in urban centers (urban exploiters). Therefore, it is likely that the 

species commonly found in urban areas and major cities of a region are the same. This 

colonization phenomenon by urban exploiters may be increased, since the effects of 

urbanization present a threat and cause displacement of native species in urban areas 

(Marzluff, 2001; McKinney, 2002; Biamonte et al., 2011). 

The majority of the studies we included in this review reported negative effects of 

urbanization on amphibians, and the minority reported positive effects. This suggests that 

according to our results, the negative effects of urbanization on amphibians overcome the 

positive effects. The type of species with higher positive reports was the exploiters, and 

there were no positive effects reported for avoider species, so the positive effects are only 

benefiting a restricted group of species. We found the same for the survivor and N/A 

species, which did have some positive effects reported, but the majority were either neutral 

or negative. 

The most common negative effect reported was a lower abundance and/or occurrence of 

amphibian species in urban sites. For example, for the salamander species Eurycea 

cirrigera, larval abundance decreased with an increase in the gray area (e.g. buildings, 

houses and streets) around studied streams, due to a low basal flux of the stream, and 

changes in the water chemistry in urban and sub-urban sites of North Carolina, USA 

(Miller et al., 2007). The same was found in Atlanta, Georgia, USA with the salamander 

Desmognathus fuscus fuscus, where urbanization produced physical instability of riparian 

habitats because of increased runoff and erosion at most disturbed sites, and for this reason 

population density was inversely proportional to the urbanization degree (Orser & Shure, 

1972). For the species Hyla arborea in Switzerland, urbanization had a negative effect on 

the occurrence in studied ponds, even within a 1 km buffer (Pellet et al., 2004), and a 

different study found that this species was not present, or that it was rare in the most 

urbanized areas of the city of Plovdiv, Bulgaria, because of a lack of suitable habitat 

(Mollov, 2005). The species Eurycea tonkawae had a significantly lower average density 

in developed areas of Texas, USA (with more than 10% of impervious surface) associated 



22 
 

 
 

with urbanization, compared to undeveloped areas (less than 10% impervious surface; 

Bowles et al., 2006). A study in the central Amazonia, in Brazil, reported 13 different 

amphibian species with a lower abundance in urban sites compared to rural sites, and five 

other species had a higher abundance in urban sites (Menin et al., 2019). 

The second most commonly reported negative effect for amphibians was lower species 

richness in urban sites, compared to less urbanized or natural sites. In a study of the larval 

amphibian community in wetlands along an urbanization gradient in central Pennsylvania, 

USA, it was found that there was a lower richness of amphibian larvae in wetlands with a 

higher level of urbanization, compared to rural wetlands, as well as a decrease in the 

occurrence of adults of the frog Rana sylvatica, and the salamanders Ambystoma 

maculatum and Ambistoma jeffersonianum (Rubbo & Kiesecker 2005). In central 

Amazonia, Brazil, researchers determined the composition and abundance of anurans in 

urban and rural sites, and reported a lower richness of species in the urban areas, with 10 

anuran species only present in the rural site and not in the urban site (Menin et al. 2019). A 

similar pattern was found in western Georgia, USA, when other researchers studied 

multiple amphibian species in watersheds distributed along different categories of 

urbanization, with a lower species richness reported for the site with a higher urbanization 

level (Barret & Guyer, 2008). 

Other common negative effects reported were a reduction in population size, lower genetic 

diversity, and mortality events. For example, in North Carolina, USA, the populations of 

Eurycea cirrigera and Desmognathus fuscus frogs decreased 12% and 9% respectively, 

from 1972 to 2000, which was associated with the conversion of natural areas into urban 

areas (Price et al. 2006), In Texas, USA, researchers also found a population decline of the 

salamander Eurycea tonkawae, which was strongly correlated with an increase in urban 

area (Bendik et al. 2014).  

In Quebec and Montreal (Canada), New York (USA), and Melbourne (Australia), four 

different studies have found a low genetic diversity, including lower allelic richness, in 

amphibian species like Litoria raniformis, Plethodon cinereus, and Desmognathus fuscus, 

mostly because of habitat fragmentation caused by urbanization, which tends to isolate 

amphibian populations (Nöel et al., 2007; Nöel & Lapointe, 2010; Munshi-South et al., 

2013; Keely et al., 2015). Finally, several authors have reported mortality events, mostly 

related to car and bicycle collisions in urban areas. For example, in Indiana, USA, authors 



23 
 

 
 

conducted surveys of multi-species road-kills in order to identify habitat characteristics 

associated with road-kills, and found that 95% of the individuals in the study were 

herpetofauna, with at least eight amphibian species found as road-kill (Glista et al., 2008). 

In Falconbridge, Australia, researchers surveyed 1.4 km of suburban streets and found that 

six frog species had high mortality due to collisions in roads, representing 33% of the local 

frog fauna (Wotherspoon & Burgin, 2011). Similarly, Laurijssens & Stark (2013) found 

that five amphibian species suffered mortality by collisions with cyclists, in a bikeway in 

the vicinity of a university area in Leeuwarden, Netherlands. 

On the other hand, the most common positive effect reported was a high abundance and/or 

occurrence of amphibians in urban sites. For example, Rana temporaria was found 

reproducing in most of the Sustainable Drainage Systems (SuDS) surveyed in Inverness, 

UK, over a period of 3 years, and the authors highlight the ability of SuDS inside the city 

to support amphibian breeding in these areas, given that they can be suitable habitats for 

reproduction (O´Brien 2015). In Australia, researchers studied amphibian assemblage 

structure in five natural and five urban sites with similar characteristics, and found that five 

out of the six amphibian species studied were only present in the urban site (Lane & 

Burgin, 2008) which might indicate that these species found benefits from the urban 

setting. Lane & Burgin (2008) hypothesize that chemicals present in urban contaminated 

waters might protect those five frog species from diseases such as chitridiomycosis, which 

can reduce mortality compared to natural sites. Menin et al. (2019) found five amphibian 

species within their study that were most common in urban areas, as compared to rural 

areas, in central Amazonia, Brazil, where authors determined the composition and 

abundance of anurans in urban and rural sites.  

The second and third most reported positive effects were bigger population size and 

colonization events, respectively. Mollov (2005) found that Bufo viridis had a larger 

population in urbanized zones compared to non-urbanized zones, showing a possible 

benefit from urbanization for this specific frog species. Konowalik et al. (2020) found that 

five amphibian species had a greater number of colonization events than extinction events 

during the study period inside urban areas. According to Konowalik et al. (2020), the 

permanency of ponds, the occurrence of those ponds near river valleys, and a high ratio of 

green area around ponds are positively correlated with amphibian species richness in the 

city. Therefore, these characteristics might be helping amphibian species colonize ponds 

within the urban limits of the city. Many studies also described positive, neutral, and 



24 
 

 
 

negative effects of urbanization for different amphibian species within the same study 

(How & Dell, 2000; Ghiurcă & Gherghel, 2008; Pulev & Sakelarieva, 2013; Entiauspe-

Neto et al., 2016; Ingle et al., 2019; Konowalik et al., 2020). For example, Ghiurcă & 

Gherghel (2008) studied the composition and distribution of the herpetofauna in urban and 

peri-urban areas in Romania, and found that four amphibian species were very common in 

highly urbanized sites and peri-urban areas, with many individuals present both in artificial 

and natural ponds, whereas four other amphibian species in the same study were rare. 

There were few individuals found only in the peri urban sites and not in the areas with a 

higher concentration of buildings and houses. Entiauspe-Neto et al. (2016) did a fauna 

inventory of amphibians and reptiles in an urban area with different levels of 

anthropogenic alteration in Rio Grande do Sul, Brazil, and found that out of 16 amphibian 

species, eight were present either in sites with low anthropogenic alteration or in sites with 

high anthropogenic alteration but in low numbers (uncommon in these areas). Other six 

amphibian species in the same study were only found in sites with no anthropogenic 

alteration, and two were abundant in sites with higher anthropogenic alteration within the 

urban site studied. This shows that different amphibian species can respond differently to 

urbanization, which is why it is important to pay attention to the general trends as well as 

to species-specific responses. 

In conclusion, our results showed that the majority of studied amphibian species (avoiders 

and survivors) inside urban areas suffered negative effects, mostly pertaining to low 

abundance, richness and smaller population size (Pellet et al., 2004; Price et al., 2006; 

Miller et al., 2007; Barret & Guyer, 2008; Menin et al., 2019). Conversely, a small group 

of species (exploiters) obtained benefits from urban sites and became the most common 

species inside urban areas (Mollov, 2005; Lane & Burguin, 2008; Menin et al., 2019). 

Notably, the large majority of urban amphibian studies came from the Global North (i.e., 

rich countries) where the amphibian diversity is lower (Duellman, 1999), and for that 

reason, our understanding of urban effects in this taxonomic group is biased to that small 

representation of species. The lack of studies in the Global South, where the majority of 

amphibian species occur, makes direct comparisons between urban and natural sites 

difficult in this area. Also the lack of long-term studies in general, which can describe the 

effects of urbanization over time, compromises our understanding of the general effects of 

urbanization on amphibians as urbanization progresses. Therefore, our recommendation 

would be to focus on this type of studies in future research on amphibian urban ecology. In 



25 
 

 
 

comparison with other taxonomic groups such as birds (Blair, 2001; Marzluff, 2001; Seress 

& Liker, 2015; Isaksson, 2018) and arthropods (Pawlikowski & Polorniecka, 1990; 

McIntyre, 2000; Raupp et al., 2010; Bang & Faeth, 2011; Fenoglio et al., 2020), our 

knowledge about the effect of urban development on amphibians is very limited, which 

reduces the potential reach of the information to impact informed decisions on their 

conservation within urban areas and to help decision makers improve urban planning in the 

future. 

Future directions for urban amphibian studies 

Our recommendation is to increase the number of studies of urban amphibian ecology in 

the Global South. More specifically, we recommend focusing on studies that make direct 

comparisons between urban and natural environments, so that the effects of urbanization 

on this group can become more directly evident. Also, it is important to focus on long-term 

studies in order to better describe the effects and responses of amphibians to urbanization 

over time. In such long-term studies, in order to make future revision on this subject easier 

and more standardized, it would be important to describe the study sites thoroughly, place 

them in an urbanization category (urban, suburban, peri-urban, rural, etc), classify the 

study species into exploiters, survivors, or avoiders as well as include the reason why the 

species was classified in a certain category. Also, we recommend clarifying if the matter 

that is being studied affects the amphibian species in a positive or negative way, to more 

clearly understand the effects of urbanization on anuran and other amphibian species.  

 

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32 
 

 
 

Tables and figures 

 

Figure 1. Percentage of urban effect studies on amphibians per country or region prior to 

November 2020 (n =104). 

 

 

 

 

 

 

 

 

 

 

 

 

Country

P
er

ce
n

ta
ge

o
f 

st
u

d
ie

s
(%

)

0

5

10

15

20

25

30

35

40

U
n

it
ed

 S
ta

te
s

A
u

st
ra

lia

B
ra

zi
l

R
o

m
an

ia

C
an

ad
a

B
u

lg
ar

y

In
d

ia

H
u

n
ga

ry

P
o

la
n

d

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n

it
ed

 K
in

gd
o

m

Sp
ai

n

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u

si
a

Ja
p

an

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ya

n
m

ar

It
al

y

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ad

ag
as

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r

N
et

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er

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n

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s

V
ie

tn
am

So
u

th
af

ri
ca

Sl
o

va
ki

a

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o

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u

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l

U
kr

ai
n

e

Sw
ed

en

A
rg

en
ti

n
a

Sw
it

ze
rl

an
d

G
er

m
an

y

M
ex

ic
o

C
o

st
a 

R
ic

a

W
es

t 
In

d
ie

s



33 
 

 
 

 

Figure 2. Percentage of urban effect studies per geographic region prior to November 2020 

(n = 104). 

 

 

 

P
er

ce
n

ta
ge

o
f 

st
u

d
ie

s
(%

)

Geographic region

0

5

10

15

20

25

30

35

40

45



34 
 

 
 

 

Figure 3. Percentage of studies including amphibians in urban areas, separated by effect 

category of urbanization on amphibian species. Percentages add up to more than 100% 

because some studies reported more than one effect in the same publication, for example, a 

positive effect for one species but a negative effect for another species. 

 

 

 

 

 

 

 

 

 

P
er

ce
n

ta
ge

o
f 

st
u

d
ie

s
(%

)

Effect category

0

10

20

30

40

50

60

70

80

Negative Neutral Positive



35 
 

 
 

 

Figure 4. Number of studies with negative, neutral and positive effects for each species 

category. 

 

 

 

 

 

 

N
u

m
b

er
o

f 
st

u
d

ie
s

Species category

0

5

10

15

20

25

30

35

40

45

Avoiders Survivors Exploiters N/A

Negative

Neutral

Positive



36 
 

 
 

 

Figure 5. Number of studies reporting each type of negative effect category, separated by 

species category (avoiders, survivors, exploiters, and N/A).  

 

 

 

 

 

 

 

 

 

0

5

10

15

20

25

30

35

40

Abundance 
and/or 

occurence

Genetic 
variability

Population size Species richness Local extintion Mortality reproduction Physiological 
damage

Avoiders

Survivors

Exploiters

N/A

N
u

m
b

er
o

f 
st

u
d

ie
s

Negative effect



37 
 

 
 

 

Figure 6. Number of studies reporting each type of possitive effect category, separated by 

species category (i.e. avoiders, survivors, exploiters, and N/A). 

 

 

 

 

 

 

 

 

 

 

 

 

0

5

10

15

20

25

Abundance/ 
occurence

Colonization Population 
size

Species 
richness

Less diseases Survival

Avoiders

Surviviors

Exploiters

N/A

N
u

m
b

er
o

f 
st

u
d

ie
s

Possitive effect



38 
 

 
 

Appendix 1  

List of studies included in the present review, found by searching the terms: “Urban 

herpetofauna”, “Urban amphibians”, “cities” AND “herpetofauna”, “cities” AND 

“amphibians”, “cities” AND “frogs”, “cities” AND “salamanders”, “cities” AND “newts”, 

“cities” AND “caecilians”. The studies included in the analysis needed to report the 

occurrence of amphibians in urban environments (presence, abundance, or compare 

between urban or another habitats) or report the effects of urbanization on amphibian 

morphology, behavior, survival, diet, or evolution. Studies that analyze the effect of 

anthropogenic pollutants in laboratories or experimentally inside cities were excluded, as 

well as reports of amphibians’ deaths in roads, if roads were outside of cities or did not 

compare city roads versus rural, or natural roads or a gradient of road density as a measure 

for urbanization. 

 

Akulenko, N. M., Dziubenko, N. V., Marushchak, O. Y., Nekrasova, O. D., & Oskyrko, O. S. 

(2019). Histological Changes in Common Toad, Bufo Bufo (Anura, Bufonidae), Liver 

Tissue Under Conditions of Anthropogenically Transformed Ecosystems. Vestnik 

Zoologii, 53(6), 501-506. 

Anderson, K. (2013). Influences Of Ecological Light Pollution On Advertisement Calls Of Spea 

Multiplicata (Amphibia: Anura: Scaphiopodidae) In Rural And Urban Populations In The 

Northern Chihuahuan Desert And An Evaluation Of Hybrid S. Bombifrons X S. 

Multiplicata Calls. 

Ascoli‐Morrete, T., Signor, E., Santos‐Pereira, M., & Zanella, N. (2019). Morphological 

abnormalities in anurans from southern Brazil. Austral Ecology, 44(6), 1025-1029. 

Barrett K, Samoray ST, Helms BS, Guyer C (2012) Southern twolined salamander diets in urban 

and forested streams in western Georgia. Southeastern Naturalist 11: 287–296. 

Barrett, K. (2009). Stream-breeding amphibian responses to land use distrubances (Doctoral 

dissertation). 

Barrett, K., & Guyer, C. (2008). Differential responses of amphibians and reptiles in riparian and 

stream habitats to land use disturbances in western Georgia, USA. Biological 

Conservation, 141(9), 2290-2300. Bendik, N. F., Sissel, B. N., Fields, J. R., O’Donnell, L. 



39 
 

 
 

J., & Sanders, M. S. (2014). Effect of urbanization on abundance of Jollyville Plateau 

salamanders (Eurycea tonkawae). Herpetological Conservation and Biology, 9(1), 206-

222. 

Boiarski, D. R., Toigo, C. M., Sobjak, T. M., Santos, A. F. P., Romão, S., & Guimarães, A. T. B. 

(2020). Assessment of antioxidant system, cholinesterase activity and histopathology in 

Lithobates catesbeianus tadpoles exposed to water from an urban 

stream. Ecotoxicology, 29(3), 314-326. 

Bókony, V., Üveges, B., Ujhegyi, N., Verebélyi, V., Nemesházi, E., Csíkvári, O., & Hettyey, A. 

(2018). Endocrine disruptors in breeding ponds and reproductive health of toads in 

agricultural, urban and natural landscapes. Science of the Total Environment, 634, 1335-

1345. 

Bókony, V., Üveges, B., Verebélyi, V., Ujhegyi, N., & Móricz, Á. M. (2019). Toads 

phenotypically adjust their chemical defences to anthropogenic habitat change. Scientific 

reports, 9(1), 1-8. 

Bowles BD, Sanders MS, Hansen RS (2006) Ecology of the Jollyville Plateau salamander 

(Eurycea tonkawae: Plethodontidae) with an assessment of the potential effects of 

urbanization. Hydrobiologia 553:111–120. 

Calderon, M. R., Almeida, C. A., González, P., & Jofré, M. B. (2019). Influence of water quality 

and habitat conditions on amphibian community metrics in rivers affected by urban 

activity. Urban Ecosystems, 22(4), 743-755. 

Ceríaco, L. M. (2012). Human attitudes towards herpetofauna: The influence of folklore and 

negative values on the conservation of amphibians and reptiles in Portugal. Journal of 

Ethnobiology and Ethnomedicine, 8(1), 1-13. 

Clark, P. J., Reed, J. M., Tavernia, B. G., Windmiller, B. S., & Regosin, J. V. (2008). 

Urbanization effects on spotted salamander and wood frog presence and abundance.  In: 

Mitchell JC, Jung Brown RE, Bartholomew B (eds) Urban herpetology. Salt Lake City, 

UT, 67-75. 

Bodin, A. A., Ferenti, S., Ianc, R & Covaciu-Marcov, S. D. (2013). Some data upon the 

herpetofauna and terrestrial isopods from Beiuş town, Romania. South Western Journal of 

Horticulture, Biology and Environment 4(2), 137-149. 



40 
 

 
 

Dawson, D. E., & Hostetler, M. E. (2008). Herpetofaunal use of edge and interior habitats in urban 

forest remnants. Urban habitats, 5(1), 103-125. 

Entiauspe-Neto, O., Perleberg, T., & de Freitas, M. A. (2016). Herpetofauna from an urban Pampa 

fragment in southern Brazil: composition, structure and conservation. Check List, 12, 1. 

Foster, B. J., Sparks, D. W., & Duchamp, J. E. (2004, January). Urban herpetology II: amphibians 

and reptiles of the Indianapolis airport conservation lands. In Proceedings of the Indiana 

Academy of Science (Vol. 113, No. 1, pp. 53-59). 

Gabor, C. R., Davis, D. R., Kim, D. S., Zabierek, K. C. & Bendik, N. F. (2018).Urbanization is 

associated with elevated corticosterone in Jollyville Plateau salamanders. Ecol. Indic. 85, 

229–235  

Gagne SA, Fahrig L (2010) Effects of time since urbanization on anuran community composition 

in remnant urban ponds. Environ Conserv 37(2):128–135. 

Garcia-Gonzalez, C., Campo, D., Pola, I. G., & Garcia-Vazquez, E. (2012). Rural road networks 

as barriers to gene flow for amphibians: Species-dependent mitigation by traffic 

calming. Landscape and Urban Planning, 104(2), 171-180. 

Gardner, C., & Jasper, L. (2009). The urban herpetofauna of Toliara, southwest 

Madagascar. Herpetology Notes, 2(1), 239-42. 

Ghiurcă, D., & Gherghel, I. (2008). Aspects concerning the herpetofauna in the city of Bacău 

(România): urban and peri-urban environments. Herpetologica, 2, 13-19. 

Glista, D. J., DeVault, T. L., & DeWoody, J. A. (2008). Vertebrate road mortality predominantly 

impacts amphibians. Herpetological conservation and Biology, 3(1), 77-87. 

Gutiérrez-Vannucchi, A. C., Rodríguez-Umaña, P., Sandoval, L., & García-Rodríguez, A. (2019). 

Variación en la actividad acústica de Hyalinobatrachium fleischmanni (Anura: 

Centrolenidae) en un ambiente urbano con diferentes niveles de ruido 

antropogénico. Revista de Biología Tropical, 67(2), 249-258. 

Hamer AJ, Organ AK (2008) Aspects of the ecology and conservation of the Growling Grass Frog 

Litoria raniformis in an urban-fringe environment, southern Victoria. Austral Zool 

34(3):393–407. 



41 
 

 
 

Hamer AJ, Parris KM (2011) Local and landscape determinants of amphibian communities in 

urban ponds. Ecol Appl 21(2):378–390. 

Herczeg D, Gallé R, Molnár N (2012) Effects of urbanization on the occurence of Anura 

assemblages in the city of Szeged (Hungary). Tiscia 39:3–8. 

Hill, J. E., Lawson, K. M., & Tuckett, Q. M. (2017). First record of a reproducing population of 

the African clawed frog Xenopus laevis Daudin, 1802 in Florida (USA). BioInvasions 

Record, 6(1). 

Hodgkison, S. C., Hero, J. M., & Warnken, J. (2007). The conservation value of suburban golf 

courses in a rapidly urbanising region of Australia. Landscape and urban planning, 79(3-4), 

323-337. 

Holtmann L, Philipp K, Becke C, Fartmann T (2017) Effects of habita and landscape quality on 

amphibian assemblages of urbanstormwater ponds. Urban Ecosyst 20:1249–1259. 

https://doi.org/10.1007/s11252-017-0677-y. 

Holzer, K. A. (2014). ‘Amphibian Use of Constructed and Remnant Wetlands in an Urban 

Landscape’, Urban Ecosystems, 17: 955–68. 

Holzer, K. A., Bayers, R. P., Nguyen, T. T., & Lawler, S. P. (2017). Habitat value of cities and 

rice paddies for amphibians in rapidly urbanizing Vietnam. Journal of Urban 

Ecology, 3(1). 

Homan, R. N., Windmiller, B. S., & Reed, J. M. (2004). Critical thresholds associated with habitat 

loss for two vernal pool‐breeding amphibians. Ecological Applications, 14(5), 1547-1553. 

Homola, J. J., Loftin, C. S., Cammen, K. M., Helbing, C. C., Birol, I., Schultz, T. F., & Kinnison, 

M. T. (2019). Replicated landscape genomics identifies evidence of local adaptation to 

urbanization in wood frogs. Journal of Heredity, 110(6), 707-719. 

How, R. A. (1998). Long-term sampling of a herpetofaunal assemblage on an isolated urban 

bushland remnant, Bold Park, Perth. Journal of the Royal Society of Western Australia, 81, 

143. 

How, R. A., & Dell, J. (2000). Ground vertebrate fauna of Perth's vegetation remnants: impact of 

170 years of urbanization. Pacific Conservation Biology, 6(3), 198-217. 



42 
 

 
 

Htay, H., & Phyoe, K. S. S. (2019). Assessment of conservation on herpetofauna species inhabited 

in some villages of Inle lake. 

Iglesias-Carrasco, M., Martín, J., & Cabido, C. (2017). Urban habitats can affect body size and 

body condition but not immune response in amphibians. Urban Ecosystems, 20(6), 1331-

1338. 

Ingle, M., Yadav, U., Bhilala, A. K., & Pawar, M. (2019). Urban Herpetofauna: A Case Study in 

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Capítulo 2. Effects of anthropogenic noise on the acoustic characteristics of a glass 

frog call in urban conditions 

 

 

 

 

 

 

 

 

 

 

 



50 
 

 
 

Abstract. Many animal groups use acoustic communication as their main form of 

communication for social interactions. Characteristics of the environment influence the 

way animals communicate acoustically. Anthropogenic noise is a new feature of the 

environment within urban areas that can make acoustic communication more difficult 

because it can overlap with animal vocalizations, producing acoustic masking. Multiple 

strategies have been used by different animals groups to avoid acoustic masking, but our 

understanding of acoustic plasticity in amphibians is limited compared to other animal 

groups. Therefore, our objective was to describe how the Fleischmann’s Glass Frog 

Hyalinobatrachium fleischmanni males avoid the effects of anthropogenic noise on the 

spectral characteristics of its advertisement calls. We selected two sites with different 

degrees of urban development. We recorded 56 calling males in total, measured 7 acoustic 

characteristics for each male, and related them to anthropogenic chronic and 

instantaneousaneous noise levels at each site. The urban site had a higher chronic noise 

level than the rural site. When related to chronic noise, both call duration and time between 

calls were longer in the urban site and the call duration and time between calls decreased as 

the chronic noise increased. Minimum frequency and frequency of maximum amplitude 

were higher at the urban site. Regarding instantaneousaneous noise, time between calls 

decreased when instantaneousaneous noise increased but the rest of the acoustic 

characteristics did not vary. We found that chronic and instantaneousaneous noise affect 

the acoustic characteristics of Fleischmann’s Glass Frog calls differently, and apparently 

for this species the chronic noise levels have more of an effect on the structure of calls. 

Key words: urbanization, anuran, amphibian, Hyalinobatrachium fleischmanni, bioacustic, 

vocalization 

Acoustic communication represents one of the main forms of communication in many 

groups of animals such as birds, mammals, amphibians, and reptiles (Ryan, 2001; 

Bradbury & Vehrencamp, 1998), and it is used in social interactions such as courtship, 

copulation, territory defense, or agoni