Diversidad-de-los-ascomicetes-marinos-y-genetica-de-la-poblaciones-de-corollospora-martima-de-las-playas-del-Golfo-de-Mexico

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UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO 
POSGRADO EN CIENCIAS BIOLÓGICAS 
INSTITUTO DE BIOLOGÍA 
ECOLOGÍA 
 
 
DIVERSIDAD DE LOS ASCOMICETES MARINOS Y GENÉTICA DE LA 
POBLACIONES DE COROLLOSPORA MARITIMA DE LAS PLAYAS DEL 
GOLFO DE MÉXICO 
TESIS 
QUE PARA OPTAR POR EL GRADO DE: 
DOCTORA EN CIENCIAS 
 
 
PRESENTA: 
PATRICIA VÉLEZ AGUILAR 
 
TUTORA PRINCIPAL DE TESIS: DRA. MARÍA DEL CARMEN AUXILIO 
GONZÁLEZ VILLASEÑOR 
 INSTITUTO DE BIOLOGÍA 
COMITÉ TUTOR: DR. JOAQUÍN CIFUENTES BLANCO 
 FACULTAD DE CIENCIAS 
DRA. MARÍA DEL ROCÍO REYES MONTES 
FACULTAD DE MEDICINA 
 
 
MÉXICO, D.F. AGOSTO 2014. 
	
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UN M¡ifj 
POSG DO ~]; 
Ciencias iológicas 
Dr. Isidro Ávila Martínez 
Director General de Administración Escolar, UNAM 
Presente 
COORDINACiÓN 
Me permito informar a usted que en la reunión del Subcomité por Campo de Conocimiento de 
Ecologla y Manejo Integral de Ecosistemas del Posgrada en Ciencias BiolOgicas, celebrada el dla 9 
de junio de 2014, se aprobó el siguiente jurado para el examen de grado de DOCTORA EN 
CIENCIAS de la alumna VÉLEZ AGUILAR PATRICIA con número de cuenta 404105178 con la tesis 
titulada: ~ Diversidad do los Ascomicetes marinos 'J genética de poblaciones de Coro llospora marítima 
de las playas del Golfo de México", realizada bajo la dirección de la DRA. MARíA DEL CARMEN 
AUXILIO GONZÁlEZ VILLASEÑOR: 
Presidente: 
Vocal: 
Secretario: 
Suplente: 
Suplente 
DR. MIGUEL ARMANDO ULLOA SOSA 
DRA. VALERIA FRANCISCA. E.L.M. SOUZA SALDIVAR 
DRA. MARIA DEL ROCIO ALICIA REYES MONTES 
DRA. TZVETANKA DIMITROVA DINKOVA 
DRA. FRANCISCA HERNANDEZ HERNÁNDEZ 
Sin otro particular, me es grato enviarle un cordial saludo. 
ATENTAMENTE 
"POR MI RAZA HABLARA EL ESPIRITU" 
Cd. Universitaria, D.F. a 6 de agosto de 201 4. 
ORA. MARíA DEL CORO ARIZMENOI ARRIAGA 
COORDINADORA DEL PROGRAMA 
c.c.p. Expediente del (la) interesado (a). 
Unidad de Posgr.!do • Coordinución del Posgrado en CicnclDs Biológicas Edificio B. I ero Pi~. Circuito dc Posgrndos ed. Univcrsltaria 
Delegación Coyoacán c.P. 0451 0 México. D.F. Tel . 5623 7002 hupJ/pchlOl.posgrndo.umun.lflx 
	
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AGRADECIMIENTOS 
 
Al Posgrado en Ciencias Biológicas, UNAM. 
 
Al CONACyT por otorgarme la beca 220357 para realizar los estudios de Doctorado en el 
periodo del 9 de agosto del 2010 al 08 de agosto del 2014. 
 
Al programa PAEP, por los fondos concedidos para participar como ponente en el Asian 
Mycological Congress with 12th Marine and Freshwater Mycology Symposium (7-11 de 
agosto 2011, Incheon, Corea del Sur), para asistir a la estancia de investigación “Revision 
of the populations of Corollospora maritima inhabiting the coastline of Japan” en el 
Fungus/Mushroom Resource and Research Center, Universidad de Tottori, Tottori, Japón 
(1 al 31 de octubre del 2012), y para asistir a la estancia de investigación “Training in 
molecular systematics of Ascomycota”, en el National Museum of Nature and Science, 
Tsukuba, Japón (30 de octubre al 30 de noviembre del 2013). 
 
A los miembros de mi Comité Tutor: Dr. Joaquín Cifuentes Blanco, Dra. María del 
Carmen González Villaseñor y Dra. María del Rocío Reyes Montes. 
 
 
 
 
 
	
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AGRADECIMIENTOS A TÍTULO PERSONAL 
 
Expreso mi gratitud a las siguientes personas e instituciones que participaron en mi formación 
académica y en el desarrollo de la presente investigación. 
• Al la Universidad Nacional Autónoma de México y al Instituto de Biología, por acogerme 
como estudiante y brindarme la infraestructura para realizar mi investigación. 
• A los miembros del jurado: Dr. Joaquín Cifuentes Blanco, Dra. Tzvetanka Dimitrova 
Dinkova, Dra. Francisca Hernández Hernández, Dra. María del Rocío Reyes Montes, Dra. 
Valeria Francisca E.L.M. Souza Saldivar y Dr. Miguel Armando Ulloa Sosa, por los 
comentarios emitidos para mejorar el presente escrito. 
• A la Dra. María del Carmen González Villaseñor por fungir como tutora principal durante 
mis estudios de doctorado, por su constante apoyo y por brindarme una invaluable 
formación integral. 
• A la Dra. Silvia Capello García, al Dr. Edmundo Rosique Gil, al Biól. Mario Eduardo Sosa 
y a la Universidad Juárez Autónoma de Tabasco, División Académica de Ciencias 
Biológicas, por su apoyo, atenciones y facilidades brindadas durante el muestreo de los 
estados de Tabasco, sur de Veracruz y Campeche. 
• A la Dra. Tzvetanka Dimitrova Dinkova por el apoyo e instrucción para la realización de la 
secuenciación y el estudio del transcriptoma de Corollospora maritima, por su amable 
tutoría y confianza brindada para realizar dicho proyecto. 
• Al Dr. Jaime Gasca Pineda por su apoyo incondicional, su asistencia durante la 
realización de la presente investigación, y sobre todo por impulsarme para alcanzar mis 
metas. 
• Al Dr. Akira Nakagiri por recibirme en su laboratorio, por compartir su extenso 
conocimiento en el área de la micología marina, por sus asesorías siempre acertadas y por 
su apoyo incondicional para formarme en la micología marina. 
• Al Dr. Tsuyoshi Hosoya por admitirme en su grupo de investigación, por instruirme con 
excelencia durante mi estancia de investigación en su laboratorio, por su apoyo y 
cordialidad para el establecimiento de una fructífera colaboración. 
• Al Dr. Richard T. Hanlin por su apoyo constante e incondicional durante esta etapa de mi 
formación como micóloga. 
• A mi familia y mis amigos por acompañarme durante este proceso. 
	
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ÍNDICE 
 
Agradecimientos……………………………………………………………………. iv 
Agradecimientos a título personal…………………………………………………... v 
 
Resumen…………………………………………………………………………….. 7 
Abstract……………………………………………………………………………... 8 
1 Introducción………………………………………………………………………… 9 
 1.1 Diversidad………………………………………………………………….... 9 
1.2 Genética de poblaciones…………………………………………………….. 11 
2 Estructura de las comunidades de los ascomicetes marinos en las playas del 
Golfo de México………………………………………….. …………………………. 18 
3 Diversidad de los ascomicetes marinos en la costa de la Isla Cozumel ………….. 40 
4 Diversidad de los ascomicetes marinos en la costa del estado de Tabasco………. 49 
5 Genética de poblaciones de Corollospora maritima.……………………………...... 60 
6 Discusión ……………….……………………………………………………………. 75 
7 Conclusiones…………………………………………………………………………. 79 
8 Literatura citada……………………………………………………………………... 81 
	
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Resumen 
 
Los ascomicetes saprobios que habitan en la zona intermareal de las playas arenosas son un 
grupo ecológico de microorganismos marinos que habitan en los espacios intersticiales que 
se forman entre o sobre los granos de arena y restos orgánicos compuestos por 
lignocelulosa nutriéndose de éstos últimos. Su diversidad taxonómica se encuentra poco 
estudiada tanto a nivel mundial como a nivel nacional, y por consecuencia, se ignora la 
magnitud y la distribución de su diversidad genética y patrones ecológicos. En México, la 
costa del Golfo de México representa un ecosistema frágil que enfrenta una problemática 
ambiental relacionada con la contaminación de agua y sedimentos, erosión litoral y pérdida 
de biodiversidad.A pesar de ello, las playas arenosas de dicho litoral, potencialmente 
albergan una diversidad valiosa de ascomicetes marinos arenícolas cuyo valor intrínseco y 
utilitario amerita su descripción, conservación y uso. Dicha diversidad se desconoce y 
posiblemente se esté perdiendo antes de su descripción y aprovechamiento. Conjuntamente 
con el desconocimiento de la diversidad taxonómica, actualmente se ignora la magnitud y 
la distribución de la diversidad genética en los hongos marinos a nivel mundial, así como 
sus patrones ecológicos. Lo anterior es resultado de la falta de diversificación en los 
estudios sobre micología marina, ya que en adición a los escasos estudios taxonómicos, no 
existe información relacionada con la ecología ni los patrones genéticos de este grupo de 
ascomicetes. El presente escrito está estructurado por artículos científicos que contribuyen a 
la solución de la problemática anteriormente descrita. Los resultados principales se 
relacionan con el registro de veintidós especies de ascomicetes en el Golfo de México, de 
las cuales, dos son nuevos registros para México. Se observaron importantes patrones 
ecológicos ligados al efecto que tienen algunas variables ambientales en la diversidad de 
estos hongos, así como el impacto negativo que tiene el deterioro en su ecosistema. En 
estudios adicionales, se registraron siete especies de estos ascomicetes en las costas de la 
Isla Cozumel y diecinueve en el litoral del estado de Tabasco, incluyendo un nuevo registro 
para México. Finalmente, con relación a su diversidad genética C. maritima obtuvo un 
valor alto y se observó que las poblaciones de esta especie en diferentes litorales se 
encuentran diferenciadas, aunque se detectó la presencia de flujo génico entre éstas 
implicando que existe dispersión trasatlántica de las ascosporas de este hongo. 
	
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Abstract 
 
The ascomycetes that inhabit in intertidal zone of sandy beaches comprise an ecological 
group of marine microscopic saprobes that live interstitially between or on the surface of 
sand grains and/or organic remains. The diversity of this group of fungi is poorly studied 
worldwide, and in Mexico. The coast of the Gulf of Mexico represents a fragile ecosystem 
facing numerous environmental problems, which are strongly related to water and 
sediments pollution, coastline erosion, and biodiversity loss. However, this deteriorated 
coastline potentially harbors a valuable diversity of marine ascomycetes which intrinsic and 
utilitarian value merits its description, conservation and usage. However, this diversity is 
still unknown and possibly being lost before its description and exploitation. Furthermore, 
along with the lack of information about its biodiversity, the amount of genetic diversity 
and its distribution is still unknown for this group of fungi, as well as its key ecological 
patterns. This scarcity of knowledge is due to the poor diversification in the investigations 
on marine mycology, since most studies have primarily focused in solving taxonomical and 
systematic problems. Especifically in Mexico, all the surveys have assessed the taxonomy 
of this group of fungi. Therefore, there is no information about the ecology or the genetic 
diversity of these organisms. The present manuscript is structured with scientific literature 
issuing the problems mentioned above. Our main results are related to the description of 
twenty-two species of marine ascomycetes from the coast of the Gulf of Mexico, of which 
two represent new records for Mexico. Additionally, we identified important ecological 
patterns concerning to the effect that some environmental variables have on the diversity, as 
well as the negative impact that anthropogenic disturbance has on these fungi. Furthermore, 
we registered seven species of ascomycetes inhabiting the coastline of Cozumel Island, in 
addition to nineteen species from the coast of Tabasco State, including one new record for 
Mexico. Finally, our results showed that the genetic diversity of the studied populations of 
C. maritima is high. Besides, the populations located in different oceans showed genetic 
structure, however we observed genetic flow between the studied populations implying that 
ascospores can travel transatlantic distances. 
	
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1 Introducción 
 
 1.1 Diversidad 
 
Las playas marinas arenosas son ecosistemas dinámicos y variables que presentan una alta 
heterogeneidad tanto temporal como espacial. Ecológicamente, son importantes para el 
procesamiento de grandes cantidades de materia orgánica y para el reciclaje de nutrimentos 
a los ecosistemas adyacentes (Schlacher et al. 2006). Además este ambiente representa el 
70% del territorio, comprendido en litorales, por lo que es el ecotono entre biomas marinos 
y terrestres más grande del mundo (Bascom 1980). 
Los ascomicetes marinos son un componente importante de la biodiversidad intersticial. 
Este grupo ecológico de hongos principalmente saprobios, habita entre o sobre los granos 
de arena y restos vegetales en las playas marinas. Están completamente adaptados al 
ecotono en el que habitan, lo cual se refleja en su morfología y en su ciclo de vida que está 
acoplado a la dinámica de las playas (Kohlmeyer y Kohlmeyer 1979). 
La importancia del estudio de los ascomicetes marinos radica en la utilidad que estos 
microorganismos tienen para el hombre y su función ecológica. Ya que estos hongos tienen 
un uso potencial como biorremediadores. Se ha comprobado experimentalmente que 
algunas especies pertenecientes a los géneros Corollospora, Varicosporina y 
Arenariomyces, son capaces de degradar compuestos como: el n-hexadecano, el 1-
hexadeceno, el pristano y el n-tetradecano, por lo que son candidatos para ser utilizados 
como organismos biorremediadores de playas contaminadas con petróleo (Kirk y Gordon 
1988). Además, se ha reportado que la micobiota marina desempeña una función ecológica 
crucial en las playas, ya que degrada la materia orgánica que contiene celulosa, lignina, 
quitina y queratina, por lo que conforman un importante eslabón de la cadena trófica 
(Kohlmeyer y Kohlmeyer 1979; Hyde et al. 1998b; Surajit et al. 2006). Otro aspecto 
relevante sobre el estudio de estos ascomicetes, es que son una fuente importante de 
sustancias químicas nuevas de interés para el hombre, por lo que representan un recurso 
económico potencial. Un ejemplo de lo anterior es la corollosporina, antibiótico que se 
aisló de la especie Corollospora maritima (Liberra et al. 1998). Asimismo, la especie C. 
	
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maritima se ha propuesto como un bioindicador de disturbios para playas turísticas 
(González y Hanlin 2010). 
Desde su descubirmiento por Kohlmeyer en 1962, las investigaciones relacionadas con 
la micobiota marina de las playas se han centrado principalmente en la realización de 
monografías de las comunidades fúngicas presentes en los litorales de los océanos: 
Pacífico, Atlántico, Índico y Ártico (Tubaki 1968; Kohlmeyer y Kohlmeyer 1971; 
Kohlmeyer 1976; Hyde 1989; Prasannarai et al. 1999; Prasannarai y Sridhar 2001; 
Enríquez et al. 2003; Zvereva 2009). En la literatura también son frecuentes los reportes en 
los que se describen especies nuevas (Kohlmeyer y Kohlmeyer 1977; Kohlmeyer 1980; 
Nakagiri 1982; Koch y Jones 1984; Koch 1986; Nakagiri y Tokura 1987; Kohlmeyer y 
Volkmann-Kohlmeyer 1989a,b, 1991b; Sundari et al. 1996; Abdel-Wahab et al. 1999; 
Hyde et al. 1999b; Whalley et al. 2000; Prasarannai y Sridhar 2001; Koch et al. 2007; 
Abdel-Wahab et al. 2009). De igual forma, algunos micólogos marinos han enfocado sus 
investigaciones en aspectos sistemáticos y taxonómicos (Kohlmeyer 1981, 1984; 
Kohlmeyer y Kohlmeyer 1977; Kohlemeyer y Volkmann-Kohlmeyer 1991; Spatafora et al. 
1998; Kohlmeyer et al. 2000; Campbell 2005; Campbell et al. 2005; Jones et al. 2009), 
siendo Corollospora el género más estudiado (Jones et al. 1982; Nakagiriy Tokura 1987; 
Kohlmeyer y Volkmann-Kohlmeyer 1987). Sin embargo, existen pocos estudios sobre la 
fisiología, bioquímica, genética y ecología de este grupo de hongos (Sguros y Simms 1964; 
Bebout et al. 1987; Rees et al. 1979; Hyde 1989; Hyde et al. 1998b; Jones 2000; Figueira y 
Barata 2007). Específicamente en México, la mayoría de los estudios son monografías que 
documentan la diversidad en playas con importancia turística ubicadas en los litorales del 
mar Caribe, Océano Pacífico y Golfo de México (Kohlmeyer 1968; Kohlmeyer y 
Kohlmeyer 1971; Kohlmeyer 1984; González y Herrera 1993; González et al. 1998; 
González et al. 2001). Concretamente para el territorio nacional del Golfo de México, los 
únicos registros existentes corresponden a escasos estudios realizados en los estados de 
Veracruz y Tabasco, con cerca de 3,000 km de costa correspondientes a dicho territorio, 
inexplorados en su mayor parte (Kohlmeyer 1968; González et al. 1998; González et al. 
2001; INEGI 2003). 
Actualmente se conoce un total de 97,330 especies de hongos en el mundo, de los cuales 
530 especies corresponden a hongos marinos y de éstas únicamente alrededor de 35 
	
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especies habitan exclusivamente en las playas. Para México, Guzmán (1998) reportó la 
cifra conservadora de 7,000 especies de hongos conocidas, de las cuales 62 corresponden a 
especies marinas, y tan sólo cerca de 28 especies fueron reportadas de ambientes costeros; 
por lo que la micología en este país se encuentra particularmente poco desarrollada (Hyde 
et al. 1998a,b; Hyde y Goh 1998; González et al. 2001; Jones et al. 2009; Kirk et al. 2009). 
Debido a la escasez de información se desconocen los patrones de distribución 
geográfica de los hongos marinos que habitan en las playas. Sin embargo, con base en los 
registros disponibles, se cree que los hongos marinos arenícolas tienen una distribución 
amplia, que va desde la zona ártica hasta la antártica, siendo más diversos en las zonas 
tropicales; incluso algunos autores han reportado que el principal factor que delimita la 
distribución de estos hongos es la temperatura, dividiéndoles en tres grupos: especies de 
zonas templadas, especies tropicales y subtropicales, y especies cosmopolitas (Kohlmeyer y 
Kohlmeyer 1971; Kohlmeyer 1976, 1984; Volkmann-Kohlmeyer y Kohlmeyer 1993). En 
México, el conocimiento sobre la distribución de este grupo ecológico de hongos es muy 
limitado, ya que únicamente se han estudiado los litorales de 11 estados de la República 
Mexicana (Kohlmeyer y Kohlmeyer 1979; González et al. 1998; Jones 2000). 
Considerando que para México los recursos biológicos son el mayor valor sobre el cual 
descansa el bienestar del país, es necesario explorar las playas del Golfo de México (Dirzo 
y Raven 1994). En dicha región la diversidad de los ascomicetes marinos se encuentra 
desconocida en su mayoría, y posiblemente amenazada por actividades antropogénicas, por 
lo que es indispensable la recolección, preservación ex situ de los ejemplares y la creación 
de una sólida base de datos, en vista de la destrucción rápida y permanente de su hábitat, y 
así apoyar otras disciplinas y enriquecer diversos estudios a posteriori (Winston 2007; 
Llorente y Ocegueda 2008). 
 
1.2 Genética de poblaciones 
 
El objetivo de la genética de poblaciones es el de cuantificar, describir y explicar la 
variación genética dentro y entre las poblaciones (Lewontin 1991; Hartl y Clark 1997), así 
como evaluar, tanto de forma experimental como de forma teórica, los mecanismos 
mediante los cuales dicha variación se origina y cambia en el tiempo y en el espacio 
	
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(Griffiths et al. 1996; Hartl y Clark 1997). A pesar de su utilidad, la genética de 
poblaciones es una disciplina que no se ha integrado homogéneamente a la micología. 
Como resultado, la variación genética y su distribución dentro de la mayoría de los 
ascomicetes (e. g. Halosphaeriales o ascomicetes marinos) permanecen en su mayor parte 
desconocidas, mientras que para otras especies con importancia para el hombre (e. g. 
Neurospora crassa, Histoplasma capsulatum y Coccidioides immitis) el avance en su 
estudio es significativo (Scherer y Magee 1990; Burt et al. 1997; Carter et al. 2001; 
Galagan et al. 2003). 
La genética de poblaciones aplicada a la micología nos permite entender los procesos 
microevolutivos de los hongos, especialmente si consideramos que las condiciones 
impuestas por el ser humano a las poblaciones fúngicas pueden resultar en una fuerte 
selección direccional. Por ésto es crucial evaluar cómo evolucionan las poblaciones en 
respuesta a diferentes escenarios (McDonald 1997). Con base en el conocimiento de la 
diversidad genética de las poblaciones fúngicas, es posible evaluar si una especie es 
introducida, e incluso determinar su centro de origen. Cuando una población nueva se 
origina a partir de pocos individuos, su diversidad genética es menor en comparación con la 
población de origen (efecto fundador), y también en comparación con otras poblaciones de 
su mismo tamaño, pero con un tiempo de colonización mayor (Jin-Yan et al. 2010). 
La magnitud y el tipo de variación genética en poblaciones naturales varía entre distintas 
especies y se encuentra principalmente influenciada por las fuerzas evolutivas. La fuente 
principal de la variación es la mutación, mientras que la endogamia y la deriva génica la 
disminuyen. La selección y el flujo génico pueden aumentar o disminuir la variación 
dependiendo de cada situación particular (Hedrick 2005). El resultado final de la magnitud 
en la variación genética en las poblaciones se debe, en gran medida, a la acción de una o 
varias fuerzas evolutivas. Asimismo, otros aspectos como la historia de vida (e.g. sistema 
reproductivo y patrones de dispersión), caracteres ecológicos (e.g. densidad poblacional y 
hábitat), procesos demográficos (e.g. cuellos de botella y explosiones demográficas), y la 
distribución geográfica, pueden también ser importantes modeladores de la variación 
genética (Frankham et al. 2002; Hedrick 2005). 
La estructura genética en las poblaciones es otro parámetro importante que la genética 
de poblaciones evalúa. Ésta puede ser afectada por factores ecológicos o demográficos 
	
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como pueden ser el tamaño de la población, el número de los individuos que contiene cada 
población, el sistema reproductivo y la capacidad de dispersión (Hartl y Clark 1997). 
Dichos factores ocasionan que haya diferencias en las frecuencias alélicas y genotípicas 
entre poblaciones. La magnitud del flujo génico es un factor determinante de la 
estructuración de las poblaciones. Cuando el flujo génico es alto, su efecto es la 
homogenización de la variación genética entre los grupos. Sin embargo cuando es bajo, el 
efecto de la deriva génica, la selección y la mutación, pueden provocar una diferenciación 
genética mayor entre las subpoblaciones (Hartl y Clark 1997; Hedrick 2005). Además, el 
flujo génico puede restringir la evolución adaptativa de una especie evitando la 
diferenciación poblacional dada por las condiciones locales, o viceversa, promover la 
evolución dispersando genes nuevos o combinaciones de genes a lo largo del área de 
distribución de una especie. El resultado evolutivo dependerá de la acción conjunta del 
flujo génico con otras fuerzas evolutivas, además de la distribución geográfica de la especie 
(Slatkin 1987). 
Como se menciona anteriormente, un aspecto esencial en el estudio de la estructura 
genética es el efecto que tienen los factores ecológicos tales como la dispersión en la 
variación de las frecuencias alélicas y genotípicas de una región geográfica a otra. En este 
sentido, se sabe que la dispersión es un proceso clave para la biología evolutiva y para la 
dinámica de las poblaciones (Clobert et al. 2001). Sin embargo, debido a que numerosos 
factores pueden influenciar el modelado de la estructura genética de laspoblaciones, las 
inferencias sobre procesos de dispersión deben basarse en el uso de métodos 
complementarios que consideren datos geográficos e históricos (Garnier et al. 2004). 
Asimismo, es necesario que en estudios futuros se integren estrechamente datos genéticos y 
ecológicos. 
La mayoría de los trabajos sobre genética de poblaciones en hongos se centran en 
especies patógenas o de interés económico. La integración de la genética de poblaciones a 
todas las áreas de la micología es fundamental, ya que nos permitirá comprender los 
procesos microevolutivos y ecológicos de los hongos. Especialmente, debido a la creciente 
degradación y fragmentación de los ecosistemas por actividades antropogénicas, es 
necesario conocer la magnitud, distribución y características de la diversidad genética de 
	
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las poblaciones naturales, para así conservar la diversidad genética como uno de los tres 
niveles fundamentales de la biodiversidad (McNeely et al. 1990). 
Actualmente, sólo existe un estudio de genética de poblaciones en ascomicetes marinos 
realizado con las levaduras Dendryphiella arenaria y D. salina provenientes de Canadá, 
California y algunas localidades en Europa, en el que se reportó una diversidad genética 
baja. Dada la época en la que se realizó el estudio mencionado, los autores usaron 
isoenzimas para evaluar indirectamente la diversidad genética. Cabe mencionar que sus 
resultados posiblemente se vieron afectados por los problemas metodológicos que implica 
el uso de esta técnica, ya que se sabe que este método sobrestima o subestima la variación 
(Michaelis et al. 1987). Por lo que es necesario realizar estudios para evaluar la magnitud, 
distribución y características de la diversidad genética de los ascomicetes que habitan en 
ambientes marinos, especialmente costeros, ya que estos últimos están sujetos a fuertes 
disturbios de origen antrópico. 
Corollospora maritima es una especie saprobia cosmopolita y dominante que habita en 
las playas de todo el mundo. Esta especie representa un recurso económico potencial por su 
utilidad en la bioprospección, como un bioindicador de disturbio y como biorremediador de 
playas contaminadas con petróleo, por lo que la comprensión de su diversidad genética es 
útil para el manejo de cepas de interés. 
Los objetivos de la presente investigación fueron: 
1) Generales: 
a. Evaluar la diversidad taxonómica de ascomicetes marinos de doce playas arenosas 
ubicadas en el Golfo de México, mediante el método de incubación de restos 
vegetales en cámara húmeda. 
b. Analizar la magnitud de la diversidad genética y su distribución en 18 poblaciones 
de C. maritima del Golfo de México, Océano Pacífico y mar Caribe. 
2) Particulares: 
a. Aislar e identificar los ascomicetes marinos registrados en las doce playas 
estudiadas. 
b. Conservar ex situ los ejemplares registrados en forma deshidratada, preparaciones 
permanentes, cultivos vivos y criocongelados, con su respectivo ADN genómico. 
	
   15	
  
c. Comparar la diversidad de los ascomicetes registrados con otros estudios realizados 
a nivel mundial. 
d. Calcular los niveles de variación genética utilizando los siguientes estimadores: 
diversidad haplotípica (h), diversidad nucleotídica (π) y el estimador de Watterson 
(θ). 
e. Determinar la estructura de la variación genética en términos de los estimadores FST. 
f. Calcular la partición de la varianza genética por medio de un análisis de AMOVA 
(Analysis of Molecular Variance). 
g. Estimar las distancias genéticas que separan a las poblaciones y determinar sus 
relaciones de similitud. 
h. Establecer las relaciones genéticas entre las poblaciones a través de un dendograma 
construido mediante el método UPGMA (Unweighted Pair Group Method with 
Arithmetic Mean) 
 
Esta tesis está constituida por cuatro artículos científicos elaborados a partir de la 
investigación aprobada por el Comité Académico, y que la autora desarrolló durante las 
Actividades Académicas y de Investigación (I-VIII); cada capítulo comprende la siguientes 
temáticas: 
 
Estructura de las comunidades de los ascomicetes marinos en las playas del Golfo de 
México 
• Se estudió la diversidad de ascomicetes en 12 playas arenosas del Golfo de México. 
• Los valores bajos de diversidad coinciden con la presencia de áreas geográficas 
impactadas por actividades humanas. 
• Los valores altos de diversidad concuerdan con la presencia de diversos ambientes 
adyacentes a la playa. 
• El CCA (análisis de correspondencia canónica) mostró que la temperatura tiene un 
efecto marcado en la distribución de estos hongos. 
• Existe una correlación positiva significativa entre la temperatura y la diversidad de 
ascomicetes marinos en las playas. 
	
   16	
  
 
Diversidad de los ascomicetes marinos en la costa de la Isla Cozumel 
• Se registraron siete especies de ascomicetes marinos en cinco playas de la Isla 
Cozumel. 
• Lindra thalassiae y Corollospora maritima fueron las especies más abundantes. 
• Los índices de diversidad variaron entre las playas estudiadas. 
• Durante la temporada de secas la abundancia incrementó. 
• Corollospora gracilis y Lulworthia grandispora son nuevos registros para la Isla 
Cozumel. 
 
Diversidad de los ascomicetes marinos en la costa del estado de Tabasco 
• Se evaluó la diversidad de los ascomicetes marinos en diez playas del estado de 
Tabasco, México. 
• Registramos un total de 20 taxa. 
• Corollospora maritima, Corollospora sp., Halenospora varia y Torpedospora radiata 
fueron las especies dominantes. 
• Ceriosporopsis capillacea representa un nuevo registro para México. 
 
Genética de poblaciones de Corollospora maritima 
• Se analizó la magnitud de la diversidad genética del ascomicete marino de distribución 
cosmopolita, Corollospora maritima. 
• Se registró una diversidad genética alta en las 18 poblaciones estudiadas. 
• Detectamos una fuerte estructuración en las poblaciones de Hawái y el mar Caribe. 
• Se detectó flujo génico entre las poblaciones estudiadas. 
• El haplotipo (del griego haploûs y del latín typus que significa huella única y se refiere 
a un grupo de alelos que segregan juntos) dominante H2 se encontró en la mayoría de 
las poblaciones exceptuando las del mar Caribe y Hawái.
	
   17	
  
2 Estructura de las comunidades de los ascomicetes marinos en las playas del 
Golfo de México 
 
Fungal Ecology 6 (2013) 513-521 
 
COMMUNITY STRUCTURE AND DIVERSITY OF MARINE ASCOMYCETES 
FROM COASTAL BEACHES OF THE SOUTHERN GULF OF MEXICO 
 
Patricia Velez, María C. González, Edmundo Rosique-Gil, Joaquín Cifuentes, María del 
Rocío Reyes-Montes, Silvia Capello-García, and Richard T. Hanlin 
 
Abstract: 
 
Diversity of marine fungi in the Gulf of Mexico remains unknown for the most part, 
therefore the geographical distribution patterns of these microorganisms are mostly 
unknown too. Twelve sandy beaches located in this sea were sampled to evaluate the 
diversity of marine fungi, revealed by fruiting on natural substrata incubated in the 
laboratory for up to 12 months. Species richness and diversity differed between beaches, 
and corresponded with the presence of main and highly polluted river mouths, nearshore 
marine environments, and core industrial and port developments. Contaminants and local 
anthropogenic activities may be reducing the diversity of marine ascomycetes. Connections 
between beaches and different nearshore habitats explain the high diversity observed, since 
they represent a varied source of substrata for decomposition and heterogeneous 
environmental conditions. We recognized four main local species distribution patterns. 
Moreover, the constrained correspondence analysis showed that temperature is a major 
environmental variable affecting the distribution of these fungi. By a linear regression we 
showed a significant relationship between temperature and diversity. 
 
Keywords: arenicolous fungi,intertidal environment, multivariate statistics, sandy beach 
ecology, saprotroph 
	
   18	
  
Introduction 
 
Marine ascomycetes are an important component of biodiversity in sandy beaches. This 
group of fungi represents an ecological assemblage of mostly saprotrophic microorganisms 
that play an active role in the ecological function of sandy beach marine ecosystems 
(Kohlmeyer and Kohlmeyer 1979; Hyde et al. 2000; Sakayaroj et al. 2004). These saprobes 
occur on different substrata rich in lignin, cellulose, or chitin (e.g., calcareous molluscan 
and crustacean exoskeletons, plant material associated with sand grains on beaches, drift 
wood, algae and seaweeds, sea grasses, and roots, stems, leaves, fruits, seeds of mangrove 
and other vascular plants) (González 2009). Other trophic levels depend on these 
saprotrophic fungi to cleave lignocellulose so it can enter the food web through 
mycophagic invertebrates and bacteria (Newell and Porter 2000). 
Worldwide only about 530 species of marine fungi are known, out of which 424 species 
are ascomycetes (Jones et al. 2009). Currently for Mexico, barely 62 species of marine 
fungi are recorded, of which 47 are ascomycetes. In the Gulf of Mexico, a total of 60 
species of marine fungi have been described, out of which 48 are ascomycetes (González 
2009, Walker and Campbell 2010). Therefore, the marine fungal diversity of Mexico, and 
of the Gulf of Mexico, remains unknown for the most part. Moreover, the geographical 
distribution patterns of this ecological group of fungi are undefined especially at a local 
scale (Kohlmeyer 1968, 1983, 1984; González and Herrera 1993; Volkmann-Kohlmeyer 
and Kohlmeyer 1993; González et al. 1998, 2001). 
The distribution of marine fungi is principally determined by the temperature and 
salinity of the water. Five temperature-determined regions are recognized: arctic, 
temperate, subtropical, tropical and Antarctic (Hughes 1974). However, local geographical 
patterns have also been reported (Nakagiri et al. 1999). Moreover, species diversity may be 
also controlled by a combination of other factors as, effects of habitats, availability of 
substrata for colonization, inhibition, competition, dissolved organic nutrients, hydrogen 
ion concentration, osmotic effects, oxygen availability, pollutants, abundance of propagules 
in the water, ability to attach to a suitable substrata, hydrostatic pressure, substrate 
specificity, etc. (Booth and Kenkel 1986; Jones 2000). 
	
   19	
  
The Gulf of Mexico is a diverse ecosystem that provides a wide array of valuable 
resources to the nations on its shores, in terms of fisheries, tourism, agriculture, trade, 
shipping, infrastructure and oil (Cato and Adams 1999). As a result of pollutant discharges, 
oil and gas development, and nutrient loading, the ecosystems of the Gulf of Mexico show 
signs of stress in coastal regions. The Mississippi-Atchafalaya River Basin and Gulf of 
Mexico hypoxic zone is the largest zone of anthropogenic coastal hypoxia in the western 
hemisphere (Birkett and Rapport 1999; Rabalais et al. 1999). 
Assessing marine fungal diversity of threatened ecosystems is an imperative task 
considering that species diversity may be declining. Furthermore, the conservation and 
utilization of this diversity requires full knowledge about the species diversity and their 
distribution, thus the study of unexplored beaches is also an important task (Das et al. 
2006). Hence, the aim of this investigation was to analyze the diversity and distribution 
patterns of marine ascomycetes inhabiting 12 sandy beaches spread along the coastline of 
the southern Gulf of Mexico, and to evaluate the effect of three environmental variables 
(mean annual temperature, average of annual rainfall and annual salinity) in their 
geographical distribution. 
 
Materials and methods 
 
Study area 
The Gulf of Mexico is bordered by the United States of America to the north (states of 
Florida, Alabama, Mississippi, Louisiana, and Texas), Mexico to the south (states of 
Tamaulipas, Veracruz, Tabasco, Campeche, and Yucatan), and the island of Cuba to the 
southeast. It measures approximately 1 600 km from east to west, 900 km from north to 
south, and has a surface area of 1 500 000 km2 (Uchupi 1975; Salvador 1991; Gore 1992). 
The Gulf of Mexico may be divided into seven provinces according to its 
physiogeographical characteristics: Gulf of Mexico Basin, Northeast Gulf of Mexico, South 
Florida Continental Shelf and Slope, Northern Gulf of Mexico, Campeche Bank, Bay of 
Campeche, Eastern Mexico Continental Shelf and Slope (Antoine 1972). The last three 
provinces comprise the Mexican Gulf of Mexico. The Campeche Bank is an extensive 
carbonate bank located to the north of the Yucatan Peninsula (Ordonez 1936). The Bay of 
	
   20	
  
Campeche is an isthmian embayment extending from the western edge of Campeche Bank 
to the offshore regions on the east of Veracruz, and it is characterized by salt domes, a 
predominance of thick terrigenous sediments, and production of large quantities of oil. The 
Eastern Mexico Continental Shelf and Slope is located between Veracruz to the south and 
the Rio Grande to the north this province spans the entire eastern shore of Mexico, and is 
characterized by sediment-covered folds that parallel the shore created by sediment-covered 
evaporites (Bryant et al. 1968). 
Water enters the Gulf of Mexico through the Yucatan Strait, circulates as the Loop 
Current, and exits through the Florida Strait eventually forming the Gulf Stream. However, 
portions of the Loop Current often break away forming eddies affecting regional current 
patterns (Nowlin 1971). 
 
Sampling and procedures 
The samplings were conducted from March 22 to April 6th 2011 during low tide. We 
studied 12 sandy beaches spread along the coast of the Mexican Gulf of Mexico (Fig 1, 
Table 1) out of which, 11 represent unexplored sites for marine fungal diversity 
assessments (González et al. 2001). The beach environment was characterized according to 
the scheme proposed by Carranza-Edwards and Caso-Chávez (1994), and a sample was 
taken in the mesobeach of each site, a region that is covered with water and is exposed to 
the air in a rhythmic and alternate way and which extends from the maximum withdrawal 
of the outflow at low tide up to the maximum inflow at high tide. Samples were collected 
randomly, and consisted of 50 sample units (su) of washed-up detritus (wood pieces, algae 
and other debris) covered with moist sand from the collecting site and placed in plastic bags 
(Ziploc®). In the laboratory, the su were incubated for up to 12 months and examined 
periodically for the presence of reproductive structures (Kohlmeyer and Kohlmeyer 1979; 
González et al. 1998). When necessary the su were moistened with artificial seawater 
(Instant Ocean® Sea Salt, USA). 
For identifying the fungi, su were examined with a stereomicroscope (Nikon SMZ1000, 
Japan), and a microscope with Nomarski differential interference contrast optics (Nikon 
Eclipse 80i, Japan). We removed ascomata from the sand grains with a sterilized needle. 
Next, ascomata were placed in a drop of distilled water on a slide, covered with a cover 
	
   21	
  
slip, and squashed. The identification of the fungi was done based on the morphology of 
reproductive structures: ascomata, asci and ascospores (Kohlmeyer and Kohlmeyer 1979, 
Kohlmeyer and Volkmann-Kohlmeyer 1991, Hyde and Sarma 2000, Jones et al. 2009). 
Only pure isolates of cultivable taxa were obtained. The specimens were dried on the 
substrate for their preservation. Also, the ascomycetes were mounted in glycerin using the 
double cover glass method (Kohlmeyer and Kohlmeyer 1972). The dried specimens, and 
slides were deposited at the Colección de Hongos del Herbario Nacional de México 
(MEXU) of Instituto de Biología, Universidad Nacional Autónoma de México.Table 1. Sampled beaches in the Mexican Gulf of Mexico, and analyzed environmental 
variables in each study site. The beach numbers refer to Figs 1, 3, and 5. 
Beaches Coordinates Mean annual 
temperature (°C × 10) 
Mean annual 
rainfall (mm) 
Mean annual 
salinity (PSS-78) 
1. Miramar 22°17'49.11"N, 
97°48'24.97"W 
238.67 95.33 36.076 
2. Escolleras 22°15'52.77"N, 
97°47'04.81"W 
238.92 94.75 36.073 
3. Tuxpan 20°58'22.32"N, 
97°18'22.32"W 
243.08 105.17 36.288 
4. Nautla 20°12'52.16"N, 
96°45'32.34"W 
262.25 128.58 36.19 
5. Boca del Río 19°07'19.97"N, 
96°06'17.11"W 
253.42 137.58 35.439 
6. Coatzacoalcos 18°09'02.60"N, 
94°29'01.95"W 
257.58 207 35.849 
Fig 1. Map of Mexico showing 
the localities in which marine 
fungi were studied (see list of 
localities in Table 1 for 
nomenclature), and further 
geographic information: mouth of 
the Panuco River (a), industrial 
and port complexes (b), mouth of 
the Tuxpan River (c), Tuxpan 
Port (d), mouth of the 
Coatzacoalcos River (e), mouth of 
the Grijalva River (f), Pantanos de 
Centla (g), and Laguna de 
Términos (h). 
 
	
   22	
  
7. Paraíso 18°26'24.88"N, 
93°13'33.34"W 
263.17 150 35.794 
8. Ciudad del 
Carmen 
18°39'55.75"N, 
91°48'38.09"W 
264.25 124.17 36.28 
9. Seyba 19°39'34.89"N, 
90°42'15.20"W 
259.58 94.5 36.481 
10. Celestún 20°51'44.13"N, 
90°24'02.02"W 
263.75 61 36.337 
11. Progreso 21°17'18.07"N, 
89°39'50.88"W 
254.25 38.83 36.484 
12. Dzilam de 
Bravo 
21°23'26.96"N, 
88°54'19.16"W 
257.75 59.92 36.392 
 
Data analysis 
The species richness (n) was considered as the number of different species in a given area. 
We quantified the presence of the different ascomycetes that developed on each sample unit 
from each of the 12 beaches studied. The frequency of occurrence was estimated from the 
number of occurrences of a particular marine fungus (as the number of samples from which 
it was found) divided by the number total of samples × 100. Diversity was estimated with 
the Shannon-Wiener species diversity index (Hʹ′). The diversity data of marine ascomycetes 
recorded from the beaches of the Gulf of Mexico was analyzed utilizing the statistical 
software R version 2.15.2 (R Development Core Team 2012), Vegan package (Oksanen et 
al. 2013). 
To define the trends within the fungal communities, and to determine which 
environmental variable is mostly defining the distribution of marine ascomycetes in the 
studied beaches, we performed a constrained correspondence analysis (CCA) (Ter Braak 
1986) with the current implementations by Legendre and Legendre (2012), using non-
correlated environmental variables and species data. CCA is a multivariate method to 
explain the relationships between biological assemblages of species and their environment. 
The method is designed to extract synthetic environmental gradients from ecological data 
sets. The gradients are the basis for succinctly describing and visualizing the differential 
habitat preferences (niches) of taxa by an ordination diagram. Besides, this method is useful 
for aquatic ecologists to investigate how a multitude of species simultaneously responds to 
external factors (Ter Braak and Verdonschot 1995). For the analysis we used three 
environmental variables (Table 1), and species data. We downloaded current bioclimatic 
	
   23	
  
variables of mean temperature, and rainfall at the highest spatial resolution (~1 km) from 
Worldclim GIS climate database, since they are biologically meaningful variables that 
capture annual ranges, seasonality and limiting factors (Hijmans et al. 2005). Also, we used 
the variable of mean annual salinity at the highest spatial resolution (0.10 grids) 
corresponding to the sea surface records (0 m), from the Gulf of Mexico Regional 
Climatology, National Oceanographic Data Center website 
(http://www.nodc.noaa.gov/OC5/regional_climate/GOMclimatology/). Species data 
consisted of the count of the presence of all ascomycetes that developed on each of the 12 
beaches studied. Additionally, we examined the effect of the most influential environmental 
variable resulting from the CCA with linear regression. The analyses were performed using 
the Vegan package (Oksanen et al. 2013) in the statistical program R version 2.15.2 (R 
Development Core Team 2012). 
 
Results 
 
Out of 600 sus examined we identified to species level 19 taxa belonging to Ascomycota 
including: 12 Halosphaeriales, 3 Lulworthiales, 1 Mycosphaerellaceae, 1 
Phaeosphaeriaceae and 2 incertae sedis. Species richness varied among the twelve studied 
beaches, and ranged from one species (Miramar and Tuxpan) to nine species (Boca del 
Río). The value of the Shannon-Wiener species diversity index (Hʹ′) was different in the 
studied beaches. The beaches of Tuxpan and Miramar yielded the lowest diversity values, 
whereas the highest diversity values corresponded to the beaches of Nautla and Progreso 
(Fig 2). The highest value of species richness was observed in the state of Veracruz, 
whereas the lowest occurred in the state of Tabasco (Fig 3). 
We grouped species based on their frequency of occurrence into three categories: 
dominant (≥50%), common (>1, <50), and rare (≤1). According to this grouping, we only 
registered one dominant species, nine common species, and 12 rare species from the 
Southern Gulf of Mexico. However, at the single beach level, this pattern was no longer 
observed, some beaches had only one dominant species present. The most frequent species 
was Corollospora maritima (56.90%), followed by Lindra thalassiae (12.43%) (Fig 3). 
 
	
   24	
  
 
Fig 2. Shannon-Wiener diversity index values obtained for each of the twelve studied 
beaches, see Table 1 for site nomenclature. 
 
 
Fig 3. Fungal communities inhabiting the studied sandy beaches in the Gulf of Mexico, 
presenting species richness and frequency of occurrence. Each species is represented as 
follows: Corollospora maritima (1), Lindra thalassiae (2), Arenariomyces triseptatus (3), 
Lindra crassa (4), Corollospora pulchella (5), Varicosporina ramulosa (6), Arenariomyces 
trifurcatus (7), Corollospora gracilis (8), Torpedospora radiata (9), unidentified 1 (10), 
	
   25	
  
unidentified 2 (11), unidentified 3 (12), Haiyanga salina (13), Lignincola laevis (14), 
Arenariomyces majusculus (15), Arenariomyces parvulus (16), Lulworthia sp. (17), 
Ceriosporopsis halima (18), Lineolata rhizophorae (19), Mycosphaerella sp. (20), 
Leptosphaerella sp. (21), and Näis inornata (22). 
 
Several fungal species detected in this study correspond with previous records for the Gulf 
of Mexico. Three species are new records for the Gulf of Mexico: Arenariomyces 
majusculus, Lindra crassa and Näis inornata. Besides, the first one mentioned above, is a 
new record for the Mexican coastline (Fig 4A). Furthermore, only the species C. maritima 
was common to all beaches, though the species Arenariomyces parvulus, unidentified 3, 
Ceriosporopsis halima, Corollospora gracilis, Leptosphaerella sp., Lineolata rhizophorae, 
Lulworthia sp., Mycosphaerella sp., and N. inornata were recorded from only one site. 
The CCA showed that temperature, rainfall, and salinity have an important influence on 
the distribution of marine ascomycetes in the studied sandy beaches of western Gulf of 
Mexico (Fig 5). However, the first variable had major effect. The three ordination axes 
explained 70.82 %, 19.81%, and 09.37% of the variance in the species data. The 
relationship between temperature and the species: Arenariomyces trifurcatus, 
Leptosphaeria sp., L. rhizophorae, Mycosphaerella sp., and N. inornata was positive. There 
was a positive relationship between average annual rainfall and the species A. majusculus, 
A. parvulus, C. gracilis and L. crassa. However, the relationship between average of annual 
rainfall and unidentified 2 was inverse (Fig 5). There was also a positive relationshipbetween salinity and the species Arenariomyces triseptatus, Corollospora pulchella, 
unidentified 1 and unidentified 3. The effect of temperature on diversity was tested further 
with a linear regression model. The regression showed a significant positive relationship 
between temperature and diversity (P = 0.02564, r 2 = 0.3475). The studied beaches also 
grouped based on the environmental variables according to their latitudinal location. From 
our studied sites, lowest latitude beaches located in the state of Campeche (Seyba) and in 
the state of Yucatan (Celestún, Progreso, and Dzilam de Bravo) showed a positive 
relationship to salinity (Fig 5). 
 
Discussion 
	
   26	
  
 
The large number of species belonging to the Halosphaeriales may be because it is the 
largest order of marine fungi (Jones et al. 2009). Moreover, some species belonging to this 
order of marine ascomycetes have the ability to use n-hexadecane, n-tetradecane, l-
hexadecene and pristane as sole carbon sources for growth. From the collected species in 
this study, A. parvulus, A. triseptatus, C. maritima, C. pulchella, and Varicosporina 
ramulosa have been reported to use such carbon sources (Kirk and Gordon 1988, Kirk et al. 
1991). So, perhaps these species are resistant to oil pollution, explaining their 
predominance in the Gulf of Mexico. Moreover, recording twenty teleomorphic species, 
and only one anamorphic species is reasonable, since out of 530 species of marine fungi, 
only 94 species represent anamorphic fungi (Jones et al. 2009). 
In the southern Gulf of Mexico we recorded one dominant species, nine common 
species, and twelve rare species. However, at the single beach level, this pattern was no 
longer observed. For example, in the beaches of Miramar and Tuxpan we recorded only one 
species. It is well known that species richness is the simplest way to describe regional 
diversity (Magurran 2004), so we can assume that the regional diversity in these two 
beaches is poor. Contrastingly, in the beaches of Boca del Río, Coatzacoalcos, Nautla and 
Progreso we observed high richness values, corresponding with the Shannon-Wiener 
species diversity index values. The variation in richness and diversity between the studied 
beaches corresponded with the presence of the main river mouths, nearshore marine 
environments, and core industrial and port developments. 
The above-mentioned main river mouths are located near the beaches where the lowest 
diversity and richness values were detected, and correspond to: Panuco River, Tuxpan 
River, and Grijalva River. These mighty rivers collect municipal and industrial wastes (i.e. 
pesticides), thus they are regarded as highly polluted rivers, representing an important entry 
of contaminants to the coast of the Gulf of Mexico (Yañez-Arancibia et al. 2009). 
Moreover, in the south of the state of Tamaulipas, and in the north of the state of Veracruz, 
the presence of industrial and port complexes, and the Tuxpan port correspondingly, have 
notably deteriorated the ecosystem (Yañez-Arancibia et al. 2009). It has been documented 
that the growing impacts of anthropogenic disturbances, have negative effects on the 
diversity of marine fungi (González and Hanlin 2010). Moreover, pesticides have been 
	
   27	
  
reported to affect the productivity of marine organisms and may ultimately be hazardous to 
human health (Sericano et al. 1990). Several surveys have described the impact of 
pollutants on freshwater fungal communities (e.g. Maltby and Booth 1991, Bärlocher 1992, 
Tsui et al. 2001). These studies revealed that freshwater fungal species show different 
sensibilities to pesticides (Chandrashekar and Kaveriappa 1994), and little tolerance to 
metal pollution (Maltby and Booth 1991, Abel and Bärlocher 1984, Chamier and Tipping 
1997). In laboratory experiments, low concentrations of Cd, Cu and Zn inhibit growth and 
reproduction of some species of aquatic hyphomycetes (Abel and Bärlocher 1984, 1988). 
Hence, it is possible that the input of municipal and industrial contaminants by the Panuco 
River, Tuxpan River and Grijalva River, and local anthropogenic activities, are reducing 
the diversity of marine ascomycetes. Nevertheless, only a limited number of studies on 
marine fungi inhabiting sandy beaches are available to provide relevant data on this issue, 
so further studies are necessary to fully evaluate this problem. 
The sandy beach environment has important connections with other nearshore habitats. 
Evidence of such connections is the occurrence of exogenous species in sandy beaches. For 
example, the core mangrove species L. laevis in the beach of Boca del Río (Jones and Pang 
2012), and the globally distributed freshwater species N. inornata in the beach of Nautla 
(Shearer 2001). Complex coastal environments, the product of the influence of different 
types of coastal water, generate high diversity of marine fungi (Nakagiri et al. 1999). 
Moreover, fungal diversity is also related to plant diversity (Tsui et al. 1998). Congruently, 
the occurrence of different nearshore habitats, including mangrove forests, shoals, lagoons, 
river mouths, swamps, the Laguna de Términos (Protected Area for flora and fauna, 
Comisión Nacional de Áreas Naturales Protegidas, federal government of Mexico), and the 
Pantanos de Centla (Biosphere reserve, UNESCO), correspond to the beaches where the 
highest richness, and diversity values were observed. These connections with highly 
conserved and biodiverse natural areas may contribute to the maintenance of the 
mycobiota, since they represent a varied source of substrata and provide heterogeneous 
conditions for the development of these ascomycetes. 
Coatzacoalcos and Boca del Río ranked among the beaches with highest species richness 
and diversity values of marine ascomycetes. However, these beaches have been hardly 
damaged by anthropogenic activities. Remarkably some of these activities such as, urban 
	
   28	
  
development, cattle ranches and sugarcane production and processing are significant 
contributors of organic matter to the area via freshwater rivers (Yañez-Arancibia et al. 
2009). It is feasible that marine fungi are involved in ameliorating pollution within 
estuarine environments (Kirk et al. 1991, Bucher et al. 2004). Since the role of this group 
of microorganisms in nature is to break down a wide range of organic matter, perhaps 
organic pollution is not as prejudicial as other pollutants (i.e. pesticides) for marine 
ascomycetes. However, long-term and high loading of organic matter can result in oxygen-
deficient conditions, and consequently hypoxic zones, which have severe consequences for 
marine life (Vaquer-Sunyer and Duarte 2008). So, if these anthropogenic activities continue 
impacting the environment, the diversity of marine ascomycetes in beaches might be 
threatened as well. 
Recording C. maritima as the most frequent species (56.90%) agrees with previous work 
on marine fungi from Mexican coastlines (González et al. 1998). Besides, this species is 
known to have a cosmopolitan distribution throughout the year, in addition to showing 
good hyphal growth and ascomata formation over a wide range of temperatures, in contrast 
to other marine fungal species (Hughes 1974, Nakagiri et al. 1999). 
A remarkable finding was the occurrence of L. thalassiae as the second most frequent 
species (12.43%). This species always associated with Thalassia testudinum leaves. This 
ascomycete has been documented as a pathogen in Sargassum spp. (Andrews 1976) 
causing the ‘raisin disease’, and in T. testudinum causing the Thalassia disease’ (Porter 
1986). The high frequency of L. thalassiae in our study perhaps indicates an outbreak of 
infectious disease in marine plant populations in the Gulf of Mexico. This matter raises 
concerns regarding the health of the marine biota, so further studies must be undertaken to 
fullyrecognize this phenomenon (Harvell et al. 1999, 2002). 
The species A. majusculus, representing a new record for Mexico, was found in 
intertidal wood remains from the state of Veracruz in the beaches of Nautla and 
Coatzacoalcos. The worldwide distribution of this fungus is not yet fully understood. 
However, this microorganism was first described from the Pacific Ocean (Kauai, Hawaii) 
(Kohlmeyer and Volkmann-Kohlmeyer 1989), and also has been documented from the 
Indian coastline (Prasannarai et al. 1999), and from the Caribbean Sea (Guantánamo, Cuba) 
(Samón-Legrá and Enríquez 2010). Additionally, it is the first time the species L. crassa 
	
   29	
  
has been recorded from the Gulf of Mexico (attached to washed-up algae from the state of 
Veracruz in the beach of Coatzacoalcos, and in the state of Yucatan in the beaches of 
Progreso and Dzilam de Bravo). This ascomycete has been reported before in the Mexican 
Caribbean (Cozumel Island) (Kohlmeyer 1984), which is connected in the south to the Gulf 
of Mexico through the Yucatan State. Since water enters the Gulf of Mexico through the 
Yucatan Strait, and circulates northward as the Loop Current, the presence of species in the 
Gulf of Mexico may be due to the dynamics of marine currents plus favorable conditions 
for its development. 
 
Fig 4. New records of marine ascomycetes in the Gulf of Mexico, including a new record 
for Mexico. (A) Ascospores of Arenariomyces majusculus stained with lactophenol-cotton 
blue; (B) Lindra crassa. Scale bar: A, 33 µm. 
 
Many authors have reported worldwide zonal maps establishing patterns in the 
geographical distribution of marine fungi (Hughes 1974; Kohlmeyer 1983; Jones and Alias 
1997). However, local scale geographical distribution patterns of marine fungi may also be 
documented. In Japan, 3 types of distribution were recognized: wide distribution 
throughout Japan, distribution mainly in northern Japan, and distribution mainly in southern 
Japan (Nakagiri et al. 1999). After analyzing our results, and previous published work done 
in the western Gulf of Mexico (compilation by González et al. 2001), we recognized 4 
main types of species distribution patterns in the coastline of the western Gulf of Mexico: 
wide distribution (C. maritima); restricted to the Yucatan Peninsula (Arenariomyces 
triseptatus); distribution associated with the occurrence of T. testudinum (L. thalassiae); 
	
   30	
  
and restricted to the south of the state of Veracruz (C. gracilis, and L. laevis). 
Understanding current species distribution patterns is key information for predicting the 
effect of future landscape changes, conservation and utilization of mycobiota. Yet more 
data are still necessary for a precise understanding of the fungal distribution in this area. 
Few studies have been conducted using statistical methods for analyzing the distribution 
patterns in aquatic fungi (i.e. Schmit and Shearer 2004, Nikolcheva and Bärlocher 2005, 
Raja et al., 2009). This is the first work testing environmental variables to explain to 
distribution of marine fungi inhabiting sandy beaches, using an ordination analysis. We 
were able to recognize several ecological patterns. Finding that mean annual temperature 
has a major impact on the occurrence of fungal communities agrees with previous 
qualitative works (Jones 1993, 2000). However, rainfall also represents an important 
environmental variable, as well as salinity. So we conclude that the species: A. trifurcatus, 
Leptosphaeria sp., L. rhizophorae, Mycosphaerella sp. and N. inornata tend to occur in 
areas with higher temperatures. Correspondingly, the distribution of the species A. 
majusculus, A. parvulus, C. gracilis, and L. crassa might be mostly determined by rainfall, 
preferring areas with high precipitation. However, the distribution of unidentified 2 is 
heavily related to areas with low levels of precipitation. In contrast, the species A. 
triseptatus, C. pulchella, unidentified 1, and unidentified 3 may rather occur in areas with 
high levels of salinity. Nonetheless, additional research must be done to fully understand 
the environmental variables affecting the distribution of these fungi. 
Twenty years ago it was inferred that out of approximately 500 species of marine fungi 
described, at least 135 were found in the tropics (Jones 1993). However, there was no 
evidence to suggest that there were more tropical than temperate marine fungi (Fröhlich 
and Hyde 1999). The positive relationship between temperature and diversity in the 
regression indicates that diversity is expected to increase as temperature increases. This 
suggests that the diversity of marine fungi inhabiting sandy beaches in tropical ecosystems 
is higher than in temperate ones. Our results strongly support this statement for sandy beach 
ecosystems. Furthermore, they also agree with prior reports stating that fungal diversity is 
estimated to be higher in tropics (Hawksorth 2001). 
 
	
   31	
  
 
Figure 5. Constrained correspondence analysis ordination biplot showing relationships 
between environmental factors (arrows), studied beaches (in black), and marine 
ascomycetes (in red). Site nomenclature corresponds to the list of localities in Table 1, and 
species designations with Fig 2. 
 
The studied beaches grouped according to their latitudinal location. Also, our findings 
resemble the three physiogeographical provinces corresponding to the western Gulf of 
Mexico (Antoine 1972). The southern beaches (Seyba, Celestún, Progreso, and Dzilam de 
Bravo; mostly physiogeographical province of Bay of Campeche) represent an arid region 
(García 1973). These beaches grouped together in the CCA analysis, exhibiting the lowest 
levels of rainfall, and high mean annual temperatures, and the highest salinity ranks. So the 
mycobiota inhabiting these beaches may tolerate elevated salinity conditions. 
 
Acknowledgements 
 
This paper constitutes a partial fulfilment of the Graduate Program in Biological Sciences 
of the National Autonomous University of Mexico. The first author acknowledges the 
fellowship provided by the Consejo Nacional de Ciencia y Tecnología (CONACyT). We 
thank the Institute of Biology, National Autonomous University of Mexico for supporting 
the fieldwork; we also want to express our gratitude to the División Académica de Ciencias 
	
   32	
  
Biológicas, Universidad Juárez Autónoma de Tabasco for the valuable help during the 
fieldwork. Additionally, we thank anonymous reviewers for their valuable comments. 
 
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3 Diversidad de los ascomicetes marinos en la costa de la Isla Cozumel 
 
Mycoscience en prensa (2014) 
 
DIVERSITY OF SAND INHABITING MARINE ASCOMYCETES IN SOME 
TOURIST BEACHES ON COZUMEL ISLAND, MEXICO 
 
Patricia Velez, María C. González, Joaquín Cifuentes, Edmundo Rosique-Gil, Richard T. 
Hanlin 
 
Abstract 
 
Globally marine fungal diversity is poorly known, especially in Mexico. We evaluated the 
diversity of marine ascomycetes on five tourist beaches on Cozumel Island in September 
2004, and in February 2007. Fifty sample units were collected randomly from each beach 
during each sampling time. Seven species were recovered, of which Lindra thalassiae and 
Corollospora maritima were the most dominant species. Corollospora gracilis and 
Lulworthia grandispora are new records for Cozumel Island. The highest diversity value 
was found in San Francisco beach, probably because the surrounding coral reefs are an 
important source of a wide variety of substrata for these fungi. 
 
Keywords: Caribbean Sea, Halosphaeriaceae, Lulworthiales, species richness 
	
   39	
  
 
Sandy beaches comprise approximately three-quarters of the world’s shorelines, and 
represent the most widely distributed intertidal habitat (Bascom 1980; Dexter 1992). This 
unstable environment provides a variety of ecological services not available through other 
ecosystems, which are linked to the inconspicuous biodiversity occurring in the interstitial 
spaces between sand grains (Brown 2001; McLachlan and Brown 2006; Schlacher et al. 
2006). Sand inhabiting marine ascomycetes are an important component of biodiversity in 
beaches. This ecological group of microorganisms comprises saprobic fungi that produce 
fruiting bodies on sand grains, and represents a central intermediary of energy flow 
between detritus and the marine fauna because they degrade substrates rich in lignin, 
cellulose, and chitin. Despite the important ecological role that marine fungi play in sandy 
beaches, information about their diversity and distribution is still lacking, especially in 
Mexican beaches (González et al. 2001; González 2009). 
Currently, about 97,330 fungal species worldwide are known (Kirk et al. 2008). Out of 
these, only 530 species are marine taxa (Jones et al. 2009). For Mexico, only 63 species of 
marine fungi have been reported (González et al. 2001; Velez et al. 2012), from which 17 
species have been registered in Cozumel Island. 
Cozumel Island is one of the main tourist destinations in the Mexican Caribbean Sea. 
Consequently, the island ecosystems, particularly on the coast, are strongly degraded by 
anthropogenic activities (Jordan 2008; Palafox-Muñoz et al. 2008). Assessing the diversity 
on anthropogenic-disturbed areas where biodiversity is most likely to be reduced is an 
imperative task. Moreover, the knowledge of marine mycobiota of Cozumel Island is 
predominantly based on the study of the western coast, therefore the eastern coast of 
Cozumel Island is nearly unexplored for marine ascomycetes (González et al. 2001). 
Hence, the aim of this study was to evaluate the diversity of marine fungi on five principal 
tourist sandy beaches on Cozumel Island, in the state of Quintana Roo, Mexico. 
Cozumel Island is located in the Caribbean Sea (20°35′24″N, 86°43′32″W) off the 
northeastern coast of Quintana Roo State, 23 km east of the mainland town of Playa del 
Carmen, approximately 230 km southwest of Cuba, and is separated from the eastern coast 
of the Yucatan Peninsula by 17.5 km. It is the largest island in the Mexican Caribbean with 
an area of 486 km2. Along the coastline of Cozumel Island, there are coral reefs, especially 
	
   40	
  
in the southwest, mangrove, and seagrass beds of Thalassia testudinum König. It has a 
warm humid climate with heavy rains in summer [AM (fi) (i)], which is normally from 
May to October (García 2004). 
We studied five principal tourist beaches on Cozumel Island: Mezcalito (20°25'26.25"N, 
86°50'32.90"W), Punta Morena (20°24'11.99"N 86°51'26.98"W), Chen Río (20°23'2.59"N, 
86°52'26.62"W), Punta Chiqueros (20°20'43.25"N, 86°54'3.53"W), and San Francisco 
(20°29'16.34"N, 86°58'6.87"W) (Fig. 1). Samplings were performed in September 2004 
(rainy season) and in February 2007 (dry season). We characterized the beach environment 
according to the scheme proposed by Carranza-Edwards and Caso-Chávez (1994). Fifty 
sample units (SU) were collected randomly from the mesobeach at each site during low 
tide, for a total of 250 SUs for each sampling time. A SU consisted of washed-up detritus 
(wood fragments, algae wrack and other debris), which was placed into Ziploc® plastic 
bags and covered with moist sand from the collecting site for transport. In the laboratory, 
each SU was incubated for up to 6 months at laboratory temperature, under 12/12 h 
(light/dark) intervals, and examined periodically to locate reproductive structures of the 
ascomycetes (Kohlmeyer and Kohlmeyer 1979). When necessary, we moistened the SU 
with artificial seawater (Instant Ocean®, Aquarium Systems, USA). 
 
 
Examination of the SUs was carried out with light microscopy to detect fungal reproductive 
structures