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Interactions Between Macrofungi and Insects via Sporocarps in Three Types of Vegetation of the Municipality of Linares, Nuevo León, Mexico

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A high diversity of insect-fungus interactions was found in the three vegetation types; these interactions are first reported from northeastern Mexico. Mushroom species grew best in autumn and 102 species were recorded; The Oak Forest (OF) obtained 52 fungi/2206 insect specimens, the Oak-Pine Forest (OPF) obtained 46/1540 and the Tamaulipas Thornscrub (MT) 37/324. The results showed that 4070 insect specimens occurred in 313 individuals of fungi and 35 fungi had 11 species of associated insects. Daedalea elegans had 1111 insect specimens and Hexagonia papyracea, Pluteus cervinus and Schizophyllum comune only 1. The beetles had 3809 specimens, Hymenoptera 21, Hemiptera 4, Diptera 3 and Lepidoptera 2. The insect Colenis sp, was present in sporocarps of 22 species of fungi and Lasius niger in 5 fungi and all the others only in 1. The OF and OPF vegetation types had a similarity of 39.2% (ISS = 0.392) followed by TT with 18.9% (ISS = 0189). The affinity matrix of the Sørensen Coefficient showed that sites 2 and 3 were close with a similarity of 28%, sites 1 and 3 had 10%. The Shannon-Wiener Index showed a high diversity of fungi for all vegetation types; the (OPF) had a diversity of 3.59, the (OF) had 3.57 and the (MT) had 3.07. Regarding the growth habit of the species, 67 were Saprotrophic (66%); 25 Mycorrhizal (25%) and 10 parasitic (9%); 49 species were not edible (48%), 27 toxic (26%), 23 edible (23%) and 3 medicinal (3%).
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Earth and Environmental Sciences Library
Sustainable
Management of
Natural Resources
Fortunato Garza-Ocañas
Editor
Diversity, Ecology, Taxonomy
and Sociology
Earth and Environmental Sciences Library
Series Editors
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mental Sciences communities are invited to share their knowledge and expertise in
the form of edited books, monographs, and conference proceedings.
Fortunato Garza-Ocañas
Editor
Sustainable Management
of Natural Resources
Diversity, Ecology, Taxonomy and Sociology
Editor
Fortunato Garza-Ocañas
Faculty of Forestry Sciences, Department
of Sylviculture
Universidad Autónoma de Nuevo León
Nuevo León, Mexico
ISSN 2730-6674 ISSN 2730-6682 (electronic)
Earth and Environmental Sciences Library
ISBN 978-3-031-33393-4 ISBN 978-3-031-33394-1 (eBook)
https://doi.org/10.1007/978-3-031-33394-1
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Survival of species is a need for humans.
This book is dedicated to the memory of
Professor Rolando Guerra González who was
a lecturer at the Faculty of Forestry Sciences
of the Universidad Autónoma de Nuevo León.
He wholeheartedly supported and contributed
to the development of many students who
became graduated professors from several
national and international universities. As a
lecturer, he always promoted that a critical
and positive mind is a needed tool for every
student to contribute to the advancement of
science in every subject.
The authors
Foreword
The Universidad Autónoma de Nuevo León (UANL) trains professionals in many
areas of science, this is in accordance with the UANLs Vision 2030 that it is oriented
to promote human values to generate education and research of quality for the benet
of society.
Our institution has high quality standards at national and international levels and
brings together the talents and work of teachers and researchers committed with
education for the development of students.
The Univers ity encourages continuous education training for teaching-research
staff as a fundamental tool to support students as well as to carry out scientic
research that impacts the society daily. In relation to forest ecosystems and
resources, it is important to produce research and technology allowing a greater
efciency for their sustainable management and conservation.
This is an alternative to generate opportunities for people living in rural and forest
areas. The new generations of forestry professionals are well trained in the sustain-
able use and management of forest resources.
The UANL has the pleasure of providing the lecturers with this book that contains
relevant and updated information regarding the manag ement, diversity, ecology,
taxonomy, and sociology of forest and people. The chapters of this book were
written by resear chers and professors of the academic body of Natural Resources
Management and Sustainability of the Faculty of Forest Sciences who, in collabo-
ration with authors from several institutions, worked together and shared their
valuable experience and knowledge on natural resources and promoted their sus-
tainable management for the benet of students and the society.
Rector Universidad Autónoma de
Nuevo León, Nuevo Leon, Mexico
Santos Guzmán López M.D., PhD.
ix
Introduction
Celebrating 40 years of the sowing of the seed, of the Faculty of Forestry Sciences
with the edition of a book, I consi der it a great success. The topics addressed
demonstrate the variety of interests, studies, and research of this faculty team, as
well as the wide range of opportunities for students. I can only thank you for the
invitation to write the introduction to this book.
For those who have known the faculty since its early days, and among whom I
count, it is a great satisfaction to see it formed as a center of excellence in the
sciences and in the management of forest resources. This Faculty had its origin in an
idea of the Rector, Dr. Alfredo Piñeyro, in 1980. Or rather three ideas: to promote
faculties of applied sciences, to initiate the training of well-qualied teache rs before
receiving the rst students, and to decentralize the University to Linares.
Other Forestry Faculties in Mexico covered the management and forestry of
temperate forests, so the rst programs of the curriculum were designed for this
region of the country: with its arid and semi-arid zones, and its temperate forests with
enormous environmental value, but with less commercial importance. The reason
was a vision to improve the management of these resources and lands in the
properties, ranches, ejidos, municipalities, and states of the region. This is how the
faculty began, with great enthusiasm: something traditional in some senses, but with
international approaches, and with a balance of women and men students not so
conventional. In the rst few years, the studies of teachers and fellows were focused
on acquiring understandings of forest ecosystems and resources, in the broad sense,
and their dynamics.
But the forest world has changed and continues to change. In the 1980s, there was
strong concern from NGOs and the public about the rates of deforestation, and
biodiversity losses, associated with forestry and agricultural practices. Governments
and international organizations were beginning to develop more appropr iate agree-
ments and policies and (little by little) carry them out. Concerns about climate
change were still limited to think tanks and a few activists. Then, new topics, not
very traditional for foresters, entered the arenas of controversy, professional prac-
tices, and (more slowly) university curricula. In many cases, these were important
and ancient issues that are just beginning to gain due recognition.
xi
xii Introduction
With the publication in August 2021 of the latest IPCC (International Panel on
Climate Change) report, this issue reaches the highest level of politic al importance,
including a recognition of the importance of natural forest ecosystems in regulating
climates. Management practices and ofcial standards have to adapt to these
realities.
Many issues that have been gaining recognition in the forestry sector have to do
with the social importance of forests, their productivity, their management, and the
division of their benets. This is well known in the eld, although not always in
universities. In February of this year, there was a Regional Consultation on Forest
Education in Latin America, supported by FAO, IUFRO, and ITTO. Its interim
report had concluded that "Forestry education in Latin America and the Caribbean is
going through an important historical moment. On the one hand, there is a constant
demand for applicants for technical, undergraduate, and postgraduate programs and
on the other, international forest policies are increasingly demanding forestry pro-
fessionals. However, the importance of forests in maintaining human well-being is
not an issue that is covered within the programs and the forest is still conceived as a
supplier of wood and its derived products.
This vision affects the image of the forestry professional and has caused other
related programs to compete with forest programs. This concern is nothing new. In
1968, just as I was managing tropical forests in Uganda, Mr. Jack Westoby,
representing the FAO Forestry Department, in a speech on forest management
goals, noted that: Contrary to what many outsiders believe, forestry is not, in its
essence, about trees. It is about people. It is about trees only so far as they serve the
needs of people. In other words, the forestry profession exists to ensure that forest
resources, ecosystems, and values continue to sustain the needs and wills of the
population in all its variety.
In this same year of 1968, I was managing tropical forests in Uganda. We use
silvicultural treatments considered excellent by the foresters of several tropical
governments in the 1950s and 1960s. We use arboricides to poison undesirable
trees to favor desirable species: practices now considered totally incompatible with
biodiversity conservation, and with todays certication.
In the next half century, many more elements have been added to the duties of
forest managers, elements not very considered in the old days. For example: gender
equity. And the United Nations Guiding Principles on Business and Human Rights,
adopted in 2011, nally provided a guide for the implementation of the 1948
Universal Declaration of Human Rights, a very relevant issue for timber companies
in their dealings with workers, neighbors, communities, and indigenous peoples.
And gender equity.
This approach is not about social forestry. It is rather a recognition that all
forestry is social. Especially in Mexico, with its high proportion of forest resources
on the lands of ejidos and communities. In some regions of the country, since the
1980s, these owners are achieving successful, productive, protable, and even
certied forestry activities and companies. Here in the north, in arid and semi-arid
areas, there are multiple resources of comm ercial value such as candelilla, oregano,
sotol, and ixtle, and multiple ofcial norms, rules, and procedures: there is a lack of
forestry initiatives so that owners can organi ze themselves to reduce their poverty
and vulnerability.
Introduction xiii
These comments go as a form of celebration, of recognizing that the eld of
training and research has diversied in the faculty, and that this book highlights
it. Also, to put on the table the new challenges of research, training, and labor market
that the forestry sector demands with its growth.
Dr. Timothy Jasper Synnott Hillary
Senior leader of the project for the foundation of the Campus Linares of the
Universidad Autónoma of Nuevo León
Contrary to what many outsiders believe,
forestry is not, in its essence, about trees. It
is about people. It is about trees only so far
as they serve the needs of people.Jack
Westoby, FAO, 1968
9
Contents
Conservation, Regeneration and Development of Species-Rich Meadows
in Flooded Areas in Northwestern Germany .... ...... ..... ...... . 1
Burghard Wittig
Population Density of the Endemic Trout
(Oncorhynchus mykiss nelsoni) and its Relationship with the Habitat
in the Sierra San Pedro Mártir, Baja California, Mexico . .......... . 11
Gorgonio Ruiz-Campos, Mariana Solís-Mendoza,
Faustino Camarena-Rosales, Asunción Andreu-Soler,
and Iván Alejandro Meza-Matty
31
Bioenergetic Potential of the Huizache Vachellia farnesiana (L.) Willd .. 4
Sandy Juliana Hernández-Mata, Fortunato Garza-Ocañas,
Horacio Villalón-Mendoza, José Rodolfo Goche-Telles,
and Artemio Carrillo-Parra
Macromycetes Associated with Three Types of Vegetation
in the Municipality of Rayones, Nuevo León ... ...... ...... ...... . 61
Karen Elisama Rivera Luna, Fortun ato Garza-Ocañas, and Inés Yañez Díaz
Social Capital in the State of Nuevo León as a Tool for Sustainable
Forest Development . ... .. .. .. .. .. .. .. ... .. .. .. .. .. .. .. ... .. 81
Horacio Villalón-Mendoza, Artemio Carrillo-Parra,
and Angélica Judith Ocampo-Ramos
xvii
Mayan Trufes: Notes on the Hypogeous and Subhypogeous
Fungi of the Yucatan Peninsula, Mexico . . . . . . . . . . . . . . . . . . . . . . . . .
Javier Isaac de la Fuente, Jesús García Jiménez,
Gonzalo Guevara Guerrero, León Esteban Ibarra-Garibay,
Fortunato Garza-Ocañas, Michael Oswaldo Uitzil-Collí,
Juan Pablo Pinzón, and Rafael Peña-Ramírez
xviii Contents
Effect of High Temperatures That Simulate Climate Change in the
Germination of Seven Species of the Tamaulipan Thornscrub .. ..... . 99
Regina Pérez-Domínguez and Wibke Himmelsbach
Presence and Importance of Mesquite Prosopis laevigata
(Humb. & Bonpl. ex Willd.) M. C. Johnst in Northeastern Mexico ..... 115
Horacio Villalón-Mendoza, Erica Esmeralda Hernández-Hernández,
and Nelson Manzanares-Miranda
Edible Macromycetes of Chihuahua. Diversity and Nutritional
Properties .. ..... ..... ..... ..... ..... ..... ...... ..... ..... 131
María Haydeé Solano Zavala, Ivette Molinar Monsivais,
David Reyes Ruvalcaba, Miroslava Quiñónez Martínez,
Irma Delia Enriquez Anchondo, and Fortunato Garza-Ocañas
Origin and Cultural Impact of Wild Chilli Pepper
(Capsicum annuum L. var. glabriusculum) in Northeastern Mexico .. ... 143
Horacio Villalón-Mendoza, Nelson Manzanares-Miranda,
Moisés Ramìrez-Meráz, Yesenia Marisol Mejorado-Martínez,
and Juan Manuel Soto-Ramos
Diversity of Macrofungi in the Forest Ecosystems of the Cumbres
National Park .. ... ... ... ... ... ... ... ... ... .... ... ... ... ... 161
Fortunato Garza-Ocañas, Miroslava Quiñónez Martínez,
and Artemio Carrillo Parra
Diversity of Symbiosis Between Species of Macrofungi and Insects
in the Temperate Forest of Iturbide, Nuevo León ... .... .... ... .... 183
Fortunato Garza-Ocañas, Gonzalo Guevara Guerrero,
Gerardo Cuellar Rodríguez, and Lourdes Garza Ocañas
Interactions Between Macrofungi and Insects via Sporocarps in Three
Types of Vegetation of the Municipality of Linares, Nuevo León,
Mexico ...... ........... .......... ........... .......... .. 223
Elisama Rivera-Luna, Fortunato Garza-Ocañas,
Humberto Quiroz Martínez, Gerardo Cuellar Rodríguez,
José Isidro Uvalle Sauceda, Ricardo Valenzuela Garza,
and Gonzalo Guevara Guerrero
Interactions Between Macrofungals and Insects in the Oak and Pine
Forest in the Municipalities of Iturbide and Galeana, Nuevo León . ... . 247
Edwin Garza López, Fortunato Garza-Ocañas, Humberto Quiroz Martínez,
Gerardo Cuellar Rodríguez, and José Isidro Uvalle Sauceda
Epilogue . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 275
Contributors
Irma Delia Enriquez Anchondo Instituto de Ciencias Biomédicas, Universidad
Autónoma de Ciudad Juárez, Ciudad Juárez, Chihuahua, Mexico
Asunción Andreu-Soler Facultad de Ciencias Marinas, Universidad Autónoma de
Baja California, Ensenada, Baja California, México
Faustino Camarena-Rosales Facultad de Ciencias, Universidad Autónoma de
Baja California, Ensenada, Baja California, México
A. Carrillo-Parra Universidad Juárez del Estado de Durango, Instituto de
Silvicultura e Industria de la Madera, Ciudad Universitaria, Durango, Durango,
Mexico
Javier Isaac de la Fuente Universidad de Quintana Roo, División de Ciencias de
la Salud, Chetumal, Quintana Roo, Mexico
Inés Yañez Díaz Laboratorio de Suelos, Facultad de Ciencias Forestales,
Universidad Autónoma de Nuevo León, Monterrey, Nuevo León, Mexico
Fortunato Garza-Ocañas Laboratorio de Suelos, Facultad de Ciencias Forestales,
Universidad Autónoma de Nuevo León, Monterrey, Nuevo León, Mexico
Universidad Autónoma de Nuevo León, Campus Linares, Facultad de Ciencias
Forestales, Linares, Nuevo León, Mexico
Laboratorio de Micología, Facultad de Ciencias Forestales Universidad Autónoma
de Nuevo León, Linares, Nuevo León, Mexico
Facultad de Ciencias Forestales, Universidad Autónoma de Nuevo León, Linares,
Nuevo León, Mexico
Ricardo Valenzuela Garza Laboratorio de Micología, Departamento de Botánica,
Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Mexico,
Mexico
J. R. Goche-Telles Universidad Juárez del Estado de Durango, Facultad de
Ciencias Forestales, Durango, Durango, Mexico
xix
s
xx Contributors
Gonzalo Guevara Guerrero Tecnológico Nacional de México, Instituto
Tecnológico de Ciudad Victoria, Ciudad Victoria, Tamaulipas, Mexico
Erica Esmeralda Hernández-Hernández Facultad de Ciencias Fo restales,
Universidad Autónoma de Nuevo León, Linares, Nuevo León, Mexico
S. J. Hernández-Mata Universidad Autónoma de Nuevo León (UANL), Facultad
de Ciencias Forestales, Linares, Nuevo León, Mexico
Wibke Himmelsbach Facultad de Ciencias Forestales, Universidad Autónoma de
Nuevo León, Linares, Nuevo León, Mexico
León Esteban Ibarra-Garibay Universidad Nacional Autónoma de Méxi co,
UMDI Juriquilla, Facultad de Ciencias, Laboratorio de Ecología de Artrópodos en
Ambientes Extremos, Juriquilla, Querétaro, Mexico
Jesús García Jiménez Tecnológico Nacional de México, Instituto Tecnológico de
Ciudad Victoria, Ciudad Victoria, Tamaulipas, Mexico
Edwin Garza López Facultad de Ciencias Forestales, Universidad Autónoma de
Nuevo León, Linares, Nuevo León, Mexico
Karen Elisama Rivera Luna Laboratorio de Micología, Facultad de Ciencias
Forestales Universidad Autónoma de Nuevo León, Linares, Nuevo León, Mexico
Humberto Quiroz Martínez Facultad de Ciencias Biológicas, Universidad
Autónoma de Nuevo León, Laboratorio de Entomología, San Ni colásdelo
Garza, Nuevo León, Mexico
Miroslava Quiñónez Martínez Instituto de Ciencias Biomédicas, Universidad
Autónoma de Ciudad Juárez, Ciudad Juárez, Chihuahua, Mexico
Departamento Forestal, Universidad Autónoma Agr aria Antonio Narro, Saltillo,
Coahuila, Mexico
Yesenia Marisol Mejorado Martínez Facultad de Ciencias Forestales,
Universidad Autónoma de Nuevo León, Linares, Nuevo León, Mexico
Horacio Villalón Mendoza Faculty of Forestry Sciences, Autonomous University
of Nuevo León, Linares, Nuevo León, Mexico
Facultad de Ciencias Forestales, Universidad Autónoma de Nuevo León, Linares,
Nuevo León, Mexico
Moisés Ramírez Meráz Facultad de Ciencias Forestales, Universidad Autónoma
de Nuevo León, Linares, Nuevo León, Mexico
Iván Alejandro Meza-Matty Instituto de Investigaciones Oceanológicas,
Universidad Autónoma de Baja California, Ensenada, Baja California, México
Nelson Manzanares Miranda Centro de Investigación en Producción
Agropecuaria, Universidad Autónoma de Nuevo León, Linares, Nuevo León,
Mexico
Contributors xxi
Ivette Molinar Monsivais Instituto de Ciencias Biomédicas, Universidad
Autónoma de Ciudad Juárez, Ciudad Juárez, Chihuahua, Mexico
Lourdes Garza Ocañas Departamento de Farmacología y Toxicología, Facultad
de Medicina, Universidad Autónoma de Nuevo León, Monterrey, Nuevo León,
Mexico
Artemio Carrillo Parra University Juárez del Estado de Durango, Instituto de
Silvicultura e Industria de la Madera, Durango, Durango, Mexico
Universidad Juárez del Estado de Durango, Instituto de Silvicultura e Industria de la
Madera, Ciudad Universitaria, Durango, Durango, Mexico
Rafael Peña-Ramírez Tecnológico Nacional de México, Instituto Tecnológico
Superior de Irapuato, Irapuato, Guanajuato, Mexico
Regina Pérez-Domínguez Facultad de Ciencias Forestales, Universidad
Autónoma de Nuevo León, Linares, Nuevo León, Mexico
Juan Pablo Pinzón Departamento de Botánica, Facultad de Medicina Veterinaria y
Zootecnia, Universidad Autónoma de Yucatán, Mérida, Yucatán, Mexico
Angélica Judith Ocampo Ramos Faculty of Forestry Sciences, Autonomous
University of Nuevo León, Linares, Nuevo León, Mexico
Juan Manuel Soto Ramos Facultad de Ciencias Forestales, Universidad
Autónoma de Nuevo León, Linares, Nuevo León, Mexico
Elisama Rivera-Luna Facultad de Ciencias Forestales, Universidad Autónoma de
Nuevo León, Linares, Nuevo León, Mexico
Gerardo Cuellar Rodríguez Laboratorio de Entomología, Facultad de Ciencias
Forestales Universidad Autónoma de Nuevo León, Linares, Nuevo León, Mexico
Facultad de Ciencias Forestales, Universidad Autónoma de Nuevo León, Linares,
Nuevo León, Mexico
Gorgonio Ruiz-Campos Facultad de Ciencias, Universidad Autónoma de Baja
California, Ensenada, Baja California, México
David Reyes Ruvalcaba Instituto de Ciencias Biomédicas, Universidad Autónoma
de Ciudad Juárez, Ciudad Juárez, Chihuahua, Mexico
José Isidro Uvalle Sauceda Facultad de Ciencias Forestales, Universidad
Autónoma de Nuevo León, Linares, Nuevo León, Mexico
Mariana Solís-Mendoza Centro de Investigación Cientíca y de Educación Supe-
rior de Ensenada, Ensenada, Baja California, México
Michael Oswaldo Uitzil-Collí Post Grado en Biociencias, Laboratorio de
Micología, Departamento de Botánica, Escuela Nacional de Ciencias Biológicas,
Instituto Politécnico Nacional, Ciudad de Mexico, Mexico
xxii Contributors
Horacio Villalón-Mendoza Facultad de Ciencias Forestales, Universidad
Autónoma de Nuevo León, Linares, Nuevo León, Mexico
Burghard Wittig Freie Universität Berlin, Berlin, Germany
María Haydeé Solano Zavala Instituto de Ciencias Biomédicas, Universidad
Autónoma de Ciudad Juárez, Ciudad Juárez, Chihuahua, Mexico
Abbreviations
BWP backwater pool
CCP channel conuence pool
CF Fixed carbon
GLD glide
gmL light
gmMa shear resistance
gmN soil nitrogen
gmR soil reaction
HHV Higher heating
LGR low gradient rife
LSP lateral scour pool
MCP mid-channel pool
PLP pluge pool
RUN run
SRN step run
STP step pool
VM Volatile material
xxiii
Interactions Between Macrofungi and
Insects via Sporocarps in Three Types
of Vegetation of the Municipality of Linares,
Nuevo León, Mexico
Elisama Rivera-Luna, Fortunato Garza-Ocañas,
Humberto Quiroz Martínez, Gerardo Cuellar Rodríguez,
José Isidro Uvalle Sauceda, Ricardo Valenzuela Garza,
and Gonzalo Guevara Guerrero
Abstract A high diversity of insect-fungus interactions was found in the three
vegetation types; these interactions are rst reported from northeastern Mexico.
Mushroom species grew best in autumn and 102 species were recorded; The Oak
Forest (OF) obtained 52 fungi/2206 insect specimens, the Oak-Pine Forest (OPF)
obtained 46/1540 and the Tamaulipas Thornscrub (MT) 37/324. The results showed
that 4070 insect specimens occurred in 313 individuals of fungi and 35 fungi had
11 species of associ ated insects. Daedalea elegans had 1111 insect specimens and
Hexagonia papyracea, Pluteus cervinus and Schizophyllum comune only 1. The
beetles had 3809 specimens, Hymenoptera 21, Hemiptera 4, Diptera 3 and Lepidop-
tera 2. The insect Colenis sp, was present in sporocarps of 22 species of fungi and
Lasius niger in 5 fungi and all the others only in 1. The OF and OPF vegetation types
had a similarity of 39.2% (ISS = 0.392) followed by TT with 18.9% (ISS = 0189).
The afnity matrix of the Sørensen Coefcient showed that sites 2 and 3 were close
with a similarity of 28%, sites 1 and 3 had 10%. The Shannon-Wiener Index showed
a high diversity of fungi for all vegetation types; the (OPF) had a diversity of 3.59,
the (OF) had 3.57 and the (MT) had 3.07. Regarding the growth habit of the species,
H. Q. Martínez
Facultad de Ciencias Biológicas, Universidad Autónoma de Nuevo León. Laboratorio de
Entomología, Ciudad Universitaria, San Nicolás de los Garza, Nuevo León, Mexico
R. V. Garza
Laboratorio de Micología, Departamento de Botánica, Escuela Nacional de Ciencias Biológicas,
Instituto Politécnico Nacional, Mexico, Mexico
G. G. Guerrero
Tecnológico Nacional de México. Instituto Tecnológico de Ciudad Victoria, Ciudad Victoria,
Tamaulipas, Mexico
© The Author(s), under exclusive license to Springer Nature Switzerland AG 2023
F. Garza-Ocañas (ed.), Sustainable Management of Natural Resources, Earth and
Environmental Sciences Library, https://doi.org/10.1007/978-3-031-33394-1_13
223
E. Rivera-Luna · F. Garza-Ocañas () ·:email: fortunatofgo@gmail.com
G. C. Rodríguez · J. I. U. Sauceda
Facultad de Ciencias Forestales, Universidad Autónoma de Nuevo León, Linares, Nuevo León,
Mexico
67 were Saprotrophic (66%); 25 Mycorrhizal (25%) and 10 parasitic (9%); 49 species
were not edible (48%), 27 toxic (26%), 23 edible (23%) and 3 medicinal (3%).
224 E. Rivera-Luna et al.
Keywords Macroycetes · Sporocarps · Insects · Seasons · Mycophagy
1 Introduction
Forest macro fungi get their food as saprobes, parasites or mycorrhizal. During the
rainy season they produce sporocarps and many species of insects eat or complete
their life cycles within these fruits. These plant-fungal-insect interactions are impor-
tant to the partners involved in these multi-interaction symbioses. Therefore, fungal
spores are dispersed by insects to different places where they will produce new
mycelium, and insects can obtain food to complete their life cycle and disperse their
offspring in the forest. There is no set of individuals, populations or species in
ecological isolation, free from interactions with other organisms or populations
(Putman 1994), but all organisms are integrated into complex ecological interac-
tions, whose higher-order dynamics (i.e. biodiversity) arise from the interactions
between their ecological and biological components (Putman 1994). The biological
relationships that can bind organisms within a community are many and varied,
many of the links are also extremely subtle or effective (Putman 1994). Many
species of fungi are associated with a variety of insects that form different types of
symbiosis (Benjamin et al. 2004). In some cases, these associations are obvious; at
other times, only exhaustive observations throughout the life cycles of the organisms
involved and careful dissection and microscopic examination reveal the presence of
an association between them (Benjamin et al. 2004). Talking about insect-fungus
relationships is not easy, not only because both groups are considered the most
diverse on the planet, but also because the interactions that occur between them can
be complex and difcult to contextualize due to the lack of information or in many
cases (Delgado and Navarrete-Heredia 2011). Insects use fungal sporocarps as food
or as sources of enzymes, this symbiosis allows insects to use nutritional resources
and help in the dispersion of fungal spores (Benjamin et al. 2004), some species of
fungi such as those of the genus Phallus, give off odors to attract ies and other
insects that feed on their sporocarps and this is how the symbiosis begins, this type of
relationship is called mycophagia (Lawrence 1989; Amat-García et al. 2004).
Mycophagia is dened as the consumption of mycelium, fruiting body, spores or
any physical structure by an insect (Lawrence 1989); Contrary to popular belief, this
dietary pattern is widely disseminated among insects, mainly in Diptera and Cole-
optera (Amat 2007). Mycophagia is the main relationship that is established between
insects and sporocarps of macromycetes, it is also responsible for shaping the
characteristics of the interaction between these two large taxa (Benjamin et al.
2004). According to the degree of association with the fungus, insects can be
categorized as: Mycetobionts: insects whose association is mandatory, usually
depend on the fungus to carry out their life cycle. They use the fungus as a place
of refuge and egg position; they are mainly found in the early stages of development
of the fungus
Interactions Between Macrofungi and Insects via Sporocarps in Three... 225
Mycetophiles: insects whose dependence on fungi is not absolute; they exhibit
some afnity with fungi, but sources of decaying organic matter can also be found in
other resources. These types of insects are usually found in intermediate and nal
stages of fungal development. Mycetogens: To this category belong insects that are
occasionally found in sporocarps; the relationship is unclear, and they usually use
the fungus as a temporary shelter. In this category it is common to nd entomophagic
insects, parasitoids and hyperparasitoids (Amat 2007). Some Coleoptera complete
their life cycle in ephemeral eshy sporocarps, carry out accelerated larval develop-
ment of about 3 to 11 days, while those associated with persistent fungi reach within
16 to 72 days; these life stories reect an adaptation to the nature of the habitat; with
these responses they exhibit well-dened patterns according to the use of the
resource or the need to face different pressures. Considering preferences Delgado
and Navarrete-Heredia (2011) recognize three levels of specicity: Polyphagia:
Insect species that feed on sporocarps of many different species of macromycetes.
Olygophagia: A species of insect that feed on sporocarps of a few species, and
usually belong to the same genus of macromycetes or to closely related genera.
Monophages: Insect species that are very selective and specic and only feed on
sporocarps of a single species. Most mycetophilous insects are polyphagous, which
has been explained by the unpredictable and effective presence of sporocarps,
especially agaric ones (Hanski 1989). In contrast, monophagous and oligophagous
species are basically found in fungi of the Family Polyporaceae, which produce
sporocarps that remain from a few months to several years (Hanski 1989). There are
few protocols available for quantitative sampling of fungal-associated insects
(Benjamin et al. 2004). The problems involve the unpredictable timing of sporocarp
appearance of some species, the microscop ic nature of others, the need to cultivate
them, and most importantly, the irregular distribution of associated arthropod prun-
ing (Benjamin et al. 2004). The research associated with the diversity of
macromycetes for the state of Nuevo Leon is very scarce, and on its associations
with other organisms it is almost nil. To determine the value of our forests it is
important to have the knowledge of what they harbor. The objective of this research
is to determine the diversity and distribution of species of macromycetes and insects
that are associated with three types of vegetation, in addition to the degree of
association of interaction between them, to observe if there are differences in
composition and diversity in each of the sites.
2 Materials and Methods
2.1 Study Area
The municipality of Linares is located southeast of the state of Nuevo León between
the geographical coordinates of 25°09' and 24°34' North latitude and 99°07' and 99°
54' longitude Oeste (García-Hernández and Jurado 2008). The study has been carried
out in three types of vegetation in three sites located in the municipality of Linares.
They are the scrub of Tamaulipas (MT) with geographical coordinates 24°47'51''N
99°32'29''W and with an altitude of 379 m. BE Oak Forest with coordinates 24°
41'13.1''N 99°42' 20.5''W and an altitude of 617 m. and Oak Pine Forest (BPE) with
coordinates 24°42'50''N 99°47'08''W at an altitude of 1345 m (Fig. 1).
226 E. Rivera-Luna et al.
Fig. 1 Location of the study areas
2.2 Collection of Macromycetes and Associated Insects
The sampling of the sporocarps was carried out during the four seasons of the year
from December 2018 to February 2020 at each of the sites. 3 random transects of
50 meters (3 × 3 × 4) were performed, that is, 3 for the 3 types of vegetation or for the
4 seasons are a total of 36 per year; the transects were randomly located at each of the
sites where the topography allowed it. Take photographs before collection are also of
greater importance for, in the case of insects, to record their degree of association
(e.g. mycetobionts) with macromycete species (Lodge et al. 2004).
The sporocarps of the mushrooms were numbered in the eld and collected in
plastic bags for transfer to the laboratory in a refrigerator so that they could arrive
without decomposing due to the heat. Once in the laboratory, one or more specimens
of each species of fungus were placed in plastic bottles of various sizes suitable for
the size of each species of mushroom, the top of the bottles was covered with a piece
of gauze xed to the mouth of the bottle with rubber garters to prevent it from falling
off. In addition, this fabric allows perspiration. The bottles wer e labeled with the
information corresponding to the fungus species, site, season of the year number of
fungi and repetition number and incubated at 25
o
C and covered to encourage insects
to emerge either as larvae or adults, monitoring of the bottles and collection of insect
specimens daily was carried out. The insects collected were placed in small plastic
bottles with 70% ethyl alcohol for conservation and subsequent identication.
Interactions Between Macrofungi and Insects via Sporocarps in Three... 227
2.3 Data Analysis
The species of macromycetes and adult insects found in each species of fungus of
each collection site were identied, when possible, they were quantied and tabu-
lated hierarchically consi dering the criteria established by Kirk et al. (2008). Dendro-
grams of similarity of the species of macromycetes found between the different types
of vegetation were made by means of a Cluster Analysis with the MVSP (Multi-
Variate Statistical Package) software, which considers the presence/absence of the
species in the different sites using the Coefcient of the Sørensen Shannon index
determined the diversity and richness of the space of each one. collection site, as well
as the entire study.
3 Results
3.1 Diversity of Macromycetes
A total of 313 specimens belonging to 102 species of 71 genera, 12 orders and
35 families belonging to the phylum Ascomycota and Basidiomycota were collected
and identied. The phylum Basidiomycota had a greater presence in the vegetation
sites with 96 of the 102 species recorded, belonging to 10 orders, 33 families and
66 genera, being the phylum with the greatest weight in all taxonomic levels
representing 94.11% of the species collected; it was followed by the phylum
Ascomycota with 6 species of 2 orders, 2 families and 5 genera (Fig. 2). The
diversity of species was observed in the different types of vegetation and the Oak
Forest had the highest number of species with 52 of the 102 collected, it was
followed by the Oak Pine Forest with 46 species and at the end the Matorral de
Tamaulipas with 37 species (Fig. 3). At all three collection sites, the phylum
Basidiomycota was of the highest ecological importance when the largest number
of species was recorded. If we consider the exclusive species for each site, that is,
those that were recorded only in each of them, the sites (BE) and (BPE) presented the
highest number of exclusive species with 24 each, and the site (MT) presented
23 species (Tables 1 and 2).
Regarding the growth habit of the species at sites 67 were saprobes representing
66% of the species, followed by the mycorrhizal with 25 species = 25% and
parasites with 10 species = 9%. As for edible, 49 species (48%) were recorded as
inedible, 27 toxic (26%), 23 edible (23%) and 3 medicinal (3%).
228 E. Rivera-Luna et al.
Fig. 2 Types of vegetation: 1. thornscrub; 2. Oak Forest; 3. Oak-pine forest
Fig. 3 Taxonomic distribution of the species
3.2 Insect Diversity
The results showed that 4070 individuals of insects were obtained from 313 individ-
uals of macromycetes. The order Coleoptera obtained the highest number with 3809
specimens, followed by the order Hymenoptera with 21 individuals, Hemiptera
4, Diptera 3, Lepidoptera 2 individuals, and insects that could not be identied
were added in a section called other (Fig. 4).
The site (BE) had the highest number of insect individuals associated with
macromycetes with 2206 of the totals of 4070, followed by the place (BPE) with
1540 insects y to the nal is the place (MT) What Records alone 324 ins cough
(Fig. 5).
(continued)
Interactions Between Macrofungi and Insects via Sporocarps in Three... 229
Table 1 Species of macromycetes exclusive to each type of vegetation: T = Thornscrubs; OF =
Oak forest; OPF = Oak-Pine forest
T OF OPF
1 Daedalea xantha (Fr.)
A. Roy & A.B. De
Amanita vaginata (Bull.)
Lam.
Amanita caesarea (Scop.) Pers.
2 Campanella sp. Armillaria mellea
(Vahl)P. Kumm.
Amanita pantherina (DC.)
Krombh.
3 Crepidotus sp. Astraeus pteridis (Shear)
Zeller
Amanita verna (Bull.) Lam.
4 Daedaleopsis confragosa
(Bolton) J.
Boletus sp. Antrodia sp.
Schröt.
5 Fuscoporia ferruginosa
(Schrad.)
Chondrostereum
purpureum (Persoon)
Auricularia auricula-judae
(Bull.) Quél.
Murrill Pouzar
6 Gloeophyllum Cortinarius sp.2 Boletus sp.2
sepiarium (Wulfen) P.
Karst.
7 Trametes variegata Entoloma sp. Calocybe cyanea Singer ex
(Berk.) Zmitr., Wasser Redhead & Singer
& Ezhov
8 Pseudofavolus tenuis Exidia glandulosa
(Bull.) Fr.
Cortinarius sp.3
(Fr.) G. Cunn.
9 Hypoxylon sp. Gymnopus erythropus Peniophora albobadia
(Pers.) Antonín, Halling
&
(Schwein.) Boidin
Noordel.
10 Annulohypoxylon Hygrocybe sp. Hypomyces chrysospermus
truncatum (Starbäck) Tul. & C. Tul.
Y.M. Ju, J.D. Rogers
& H.M. Hsieh
11 Inocutis sp. Inocybe geophylla
(Sowerby) P. Kumm.
Inocybe sp.
12 Lysurus
periphragmoides
(Klotzsch) Dring
Lentinus tigrinus
(Bulliard)Fr.
Irpex lacteus (Fr.) Fr.
13 Neofavolus alveolaris (DC.)
Sotome & T. Hatt.
Mycena margarita
(Murrill) Murrill
Lactarius indigo (Schweinitz)
Kuntze
14 Poria sp. Panaeolina foenisecii
(Pers.) Maire
Laetiporus sulphureus (Bull.)
Murrill
15 Psathyrella candolleana (Fr.)
Maire
Panaeolus antillarum
(Fr.) Dennis
Panus neostrigosus Drechsler-
Santos & Wartchow
16 Psathyrella sp. Panellus stipticus (Bull.)
Fr. Karst.
Zhuliangomyces illinitus (Fr.)
Redhead
17 Trametes hispida
Bagl.
Peniophora quercina
(Pers.) Cooke
Hygrocybe ovina (Bull.)
Kühner
230 E. Rivera-Luna et al.
Table 1 (continued)
T OF OPF
18 Tremella lutescens
Pers.
Phaeocollybia sp. Omphalotus subilludens
(Murrill) H.E. Bigelow
19 Trametes occidentalis
(Klotzsch)Fr.
Pluteus longistriatus
(Peck) Peck
Phyllotopsis nidulans (Pers.)
Singer
20 Trichaptum biforme
(Fries) Ryvarden
Pluteus sp. Russula brevipes Peck
21 Tulostoma sp. Pluteus sp.2 Russula cyanoxantha
(Schaeff.) Fr.
22 Ustulina deusta
(Hoffm.) Maire
Pycnoporus sp. Russula mexicana Burl.
23 Xylaria hypoxylon (L.) Grev. Russula delica Fr. Russula sp.
24 Scleroderma
citrinum Pers.
Xerocomus subtomentosus
(L.) Quél.
3.3 Insect-Fungus Interactions
Of the 102 species of macromycetes identied, 35 of them presented some type of
association with insect species, so Daedalea elegans recorded the highest number of
insect individuals with 1111 of the 4070 collected, and, on the contrary, the
macromycete species that had the lowest number of associated insects were:
Hexagonia papyracea, Pluteus cervinus and Schizophyllum commune with a single
insect (Figs. 6 and 7).
As already mentioned, the order Coleoptera is the most abundant represented by
3809 individuals, where the families Leiodidae and Tenebrionidae are strongly
associated with the species of macromycetes collected, presenting a degree of
association or mycetobiont type or primary mycophagia since the Coleoptera com-
pleted thier life cycle in the fruiting body of the fungus uses it as a place for
oviposition creating galleries, and small chambers to deposit its waste. The order
Hymenoptera had 21 individuals, where the family Formicidae was present with the
genus Lasius, this genus was recorded forming a type of association Mycetogena.
The Order Hemiptera recorded a species of the Family Aradidae that had an
association of Micetogenus with the species Hexagonia tenui s and Stereum
complicatum. For the Order Diptera, Musca domestica was recorded as micetophillic
associated with Lysurus periphragmoides collected in the MT. Of the 11 insect
species identied, 5 presented a degree of mycetobiont-like association with
macromycete species, where we can nd Colenis sp., Neomida bicornis,
N. haemorrhoidalis, Diaperis sp. and D. rupes; Prometopia sp. and Musca
domestica had a mychastophile association, a type of Mycetogenic association
consisted of Lasius niger, Hemiptera of the family Aradidae, and Ithycerus sp., of
the order Arachnida of the family Ixodidae (Table 3).
Family Species Habit Edibility
xx
x x
x
x
(continued)
Interactions Between Macrofungi and Insects via Sporocarps in Three... 231
Table 2 Diversity of species, growing habit and edibility in each type of vegetation
Sites
TT BE BPE
Xylariaceae Annulohypoxylon
thouarsianum (Lév.) Y.M. Ju,
J.D. Rogers & H.M. Hsieh
S Not edible
Annulohypoxylon truncatum
(Starbäck) Y.M.
Ju, J.D. Rogers &
H.M. Hsieh
S Not edible x
Hypoxylon sp. S Not edible x
Ustulina deusta
(Hoffm.) Maire
S Not edible x
Xylaria hypoxylon
(L.) Grev.
S Medicinal x
Hypocreaceae Hypomyces chrysospermus
Tul. & C. Tul.
P Not edible x
Tremellaceae Tremella lutescens Pers. S Edible x
Agaricaceae Cyathus stercoreus
(Schwein.) By Toni
S Not edible
Tulostoma sp. M Not edible x
Amanitaceae Amanita caesarea
(Scop.) Pers.
M Edible x
Amanita pantherina (DC.)
Krombh.
M Toxic x
Amanita verna
(Bull.) Lam.
M Toxic x
Amanita vaginata (Bull.)
Lam.
M Toxic
Zhuliangomyces illinitus (Fr.)
Redhead
M Edible x
Cortinariaceae Cortinarius sp. M Toxic x
Cortinarius sp.2 M Toxic x
Cortinarius sp.3 M Toxic x
Phaeocollybia sp. M Toxic x
Cyphellaceae Chondrostereum purpureum
(Persoon) Pouzar
S Not edible x
Entolomataceae Entoloma sp. S Toxic x
Hygrophoraceae Hygrocybe sp. S Toxic x
Hygrocybe ovina (Bull.)
Kühner
M Toxic x
Inocybaceae Crepidotus sp. S Not edible x
Inocybe geophylla (Sowerby)
P.
Kumm.
MToxic x
Inocybe sp. M Toxic x
Lycoperdaceae Apioperdon pyriforme
(Schaeff.) Vizzini
S Toxic x
Family Species Habit Edibility
x
x
x
x
x x
x x
x
(continued)
232 E. Rivera-Luna et al.
Table 2 (continued)
Sites
TT BE BPE
Lyophyllaceae Calocybe cyanea Singer ex
Redhead &
Singer
M Edible x
Marasmiaceae Campanella sp. S Not edible x
Tetrapyrgos nigripes (Fr.)
E. Horak
S Not edible x
Mycenaceae Mycena margarita (Murrill)
Murrill
S Toxic x
Panellus stipticus
(Bull.) Fr. Karst.
S Not edible x
Omphalotaceae Gymnopus erythropus (Pers.)
Antonín, Halling & Noordel.
S Toxic x
Omphalotus subilludens
(Murrill) H.E.
Bigelow
M Toxic x
Phyllotopsidace ae Phyllotopsis nidulans (Pers.)
Singer
S Edible x
Physalacriaceae Armillaria mellea
(Vahl)P. Kumm.
P Edible x
Desarmillaria tabescens
(Scop.) R.A. Koch
& Aime
S Edible x
Oudemansiella melanotricha
(Dörfelt)M.M.
Moser
S Edible x
Pleurotaceae Resupinatus alboniger (Pat.)
Singer
S Not edible x
Pluteaceae Pluteus cervinus
(Schaeff.) Kumm.
S Toxic
Pluteus longistriatus
(Peck) Peck
S Toxic x
Pluteus sp. S Toxic x
Pluteus sp.2 S Toxic x
Psathyrellaceae Coprinopsis lagopus (Fr.)
Redhead, Vilgalys &
Moncalvo
S Toxic
Coprinopsis nivea (Pers.)
Redhead, Vilgalys &
Moncalvo
S Toxic x
Panaeolina foenisecii (Pers.)
Maire
S Not edible x
Panaeolus antillarum (Fr.)
Dennis
S Toxic x
Psathyrella candolleana (Fr.)
Maire
SNot edible x
Psathyrella sp. S Not edible x
Family Species Habit Edibility
x x
x x
x
x x
x x x
x x
x x
x
x
(continued)
Interactions Between Macrofungióand Insects via Sporocarps in Three... 233
Table 2 (continued)
Sites
TT BE BPE
Schizophyllacea e Schizophyllum commune Fr. S Edible
Strophariaceae Deconica coprophila (Bull.)
Fr. Kumm.
S Toxic
Auriculariaceae Auricularia auricula-judae
(Bull.) Quél..
S Edible x
Exidia glandulosa
(Bull.) Fr.
S Not edible x
Boletaceae Boletus sp. M Not edible x
Boletus sp.2 M Not edible x
Xerocomus subtomentosus
(L.) Quél.
M Edible x
Sclerodermatac eae Scleroderma citrinum Pers. S Toxic x
Gloeophyllaceae Gloeophyllum sepiarium
(Wulfen) P. Karst.
S Not edible x
Hymenochaetac eae Fulvifomes sp. P Not edible x
Fuscoporia ferruginosa
(Schrad.) Murrill
P Not edible x
Hydnoporia olivacea
(Schwein.)
Teixeira
P Not edible x
Inocutis sp. S Not edible x
Phellinus gilvus
(Schwein.) Pat.
P Not edible
Phellinus rimosus (Berk.)
Pilát
P Not edible
Trichaptum biforme (Fries)
Ryvarden
S Not edible x
Phellinus rimosus (Berk.)
Pilát
P Not edible
Phallaceae Lysurus periphragmoides
(Klotzsch)Dring
M Edible x
Cerrenaceae Cerrena hydnoides (Sw.)
Zmitr.
S Not edible
Fomitopsidacea e Antrodia sp. S Not edible x
Daedalea xantha (Fr.) A. Roy
&
A.B. De
S Not edible x
Gloeophyllaceae Heliocybe sulcata (Berk.)
Redhead
& Ginns
S Edible x
Irpicaceae Byssomerulius corium (Pers.)
Parmasto
S Not edible x
Irpex lacteus (Fr.) Fr. S Not edible x
Laetiporaceae Laetiporus sulphureus (Bull.)
Murrill
S Edible x
Family Species Habit Edibility
x
x x x
x
x x
x x
x
x x
x x
(continued)
234 E. Rivera-Luna et al.
Table 2 (continued)
Sites
TT BE BPE
Panaceae Panus neostrigosus
Drechsler-Santos &
Wartchow
S Edible x
Polyporaceae Cerioporus mollis (Sommerf.)
Zmitr.
& Kovalenko
S Not edible x
Daedaleopsis confragosa
(Bolton) J.
Schröt.
S Not edible x
Funalia hispida (Bagl.) M.M.
Chen
S Not edible x
Lentinus arcularius
(Batsch)Fr.
S Not edible
Lentinus crinitus
(L.) Fr.
S Edible x
Lentinus tigrinus
(Bulliard)Fr.
S Edible x
Neofavolus alveolaris (DC.)
Sotome & T.
Hatt.
S Edible x
Perenniporia ohiensis (Berk.)
Ryvarden
S Not edible
Poria sp. S Not edible x
Pseudofavolus tenuis (Fr.) G.
Cunn.,
S Not edible x
Pycnoporus sp. S Medicinal x
Pycnoporus sanguineus (L.)
Murrill
S Medicinal
Trametes elegans (Spreng.)
Fr.
S Not edible x
Trametes hirsuta
(Wulfen) Pilát
S Not edible
Trametes hirta (P. Beauv.)
Zmitr.,
Wasser & Ezhov
S Not edible
Trametes occidentalis Fr. S Not edible x
Trametes variegata (Berk.)
Zmitr., Wasser & Ezhov
S Not edible x
Trametes occidentalis Fr. S Not edible x
Peniophoraceae Peniophora albobadia
(Schwein.) Boidin
S Not edible x
Peniophora quercina (Pers.)
Cooke
S Not edible x
Family Species Habit Edibility
x
x x x
x
Interactions Between Macrofungi and Insects via Sporocarps in Three...235
Table 2 (continued)
Sites
TT BE BPE
Russulaceae Lactarius indigo (Schweinitz)
Kuntze
M Edible
Russula brevipes
Peck
M Edible x
Russula cyanoxantha
(Schaeff.) Fr.
M Edible x
Russula delica Fr. M Edible x
Russula mexicana Burl. M Edible x
Russula sp. M Not edible x
Stereaceae Stereum complicatum (Fr.)
Fr.
S Not edible x
Stereum ostrea (Blume &
T. Nees) Fr.
S Toxic
Diplocystidiacea eAstraeus hygrometricus
(Pers.) Morgan
S Toxic x
Astraeus pteridis
(Shear) Zeller
S Not edible x
Edibility: C = edible, NC = Inedible, T = toxic, M = medicinal.
Habit: S = Saprotrophic, M = Mycorrhizal, P = Parasite
Fig. 4 Number of species of macromycetes belonging to the phylum Ascomycota and
Basidiomycota recorded in each of the sites
236 E. Rivera-Luna et al.
Fig. 5 Number of insect specimens collected in each order
Fig. 6 Number of insects per site
3.4 Diversity of Macro Fungal Species by Season
The diversity of macromycetes was observed at the collection sites for each of the
seasons of the year, the results showed that the diversity in autumn (September
21, 2019 - December 20, 2019) was greater with 54 species and was followed by
spring (March 21, 2019 - June 20, 2019) with 36 species, winter (December 21, 2018
- March 20, 2019) with 34 species and the end of summer (June 21, 2019 -
September 20, 2019) with 25 species. Only the exclusive species for each season
were considered, that is, those that were recorded for each of them, and in the same
way the season presented the largest number of exclusive autumn species with
34 (i.e. Amanita caesarea, A. pantherina, A. verna, Amanitopsis vaginata,
Armillaria mellea, Astraeus pteridis, Auricularia auricula, Boletus sp.2, Calocybe
cyanea, Cortinarius sp. , Cortinarius sp.2, Cortinarius sp.3, Cyathus stercoreus,
Entoloma sp., Exidia glandulosa, Gloeophyllum sepiarium, Gymnopus erythropus,
Hypomyces chrysospermus, Inocybe geophylla, Inocybe sp., Lactarius indigo.
Limacella illinita, Lysurus periphragmoides, Neohygrocybe ovina, Omphalotus
subilludens, Panellus stipticus, Pluteus sp., Pluteus sp. 2, Russula sp., R. brevipes,
R. cyanoxantha, R. delica, R. mexicana and Xerocomus subtomentosus), winter
recorded 16 species (i.e. Antrodia sp., Byssomerulius corium, Campanella sp.,
Chondrostereum purpureum, Crepidotus sp. , Daedalea confragosa,
Dendropeniophora albobadia, Hydnochaete olivacea, Hypoxylon sp., Inocutis
sp. , Lentinus strigosus, L. tigrinus, Peniophora quercina, Phellinus gilvus,
Phyllotopsis nidulans and Trichaptum biforme), spring 15 (i.e. Fulvifomes sp.,
Hexagonia papyracea, Laetiporus sulphureus, Panaeolus antillarum, Polyporus
alveolaris, Poria sp., Psathyrella condolleana, Psathyrella sp. , Pycnoporus sp. ,
Interactions Between Macrofungi and Insects via Sporocarps in Three... 237
Fig. 7 Interaction between macromycetes-insect species (left) and other associated arthropods
(right)
Family Species Specicity Associated fungi Category 1 2 3
(continued)
238 E. Rivera-Luna et al.
Table 3 Insects of each type of vegetation and food specicity in each site
Sites
Araridae ND Polyphagy Pseudofavolus
tenuis
Mycetogenic *
Polyphagy Stereum
complicatum
Mycetogenic *
Formicidae Lasius niger Polyphagy Fuscoporia
ferruginosa
Mycetogenic *
Trametes hirta Mycetogeni c *
Pseudofavolus
tenuis
Mycetogenic *
Lentinus tigrinus Mycetogenic *
Pycnoporus
sanguineus
Mycetogenic *
Curculionidae Ithycerus sp. Polyphagy Byssomerulius
corium
Mycetogenic *
Leiodidae Colenis sp Oligophagy Antrodia sp. Mycetobiont *
Byssomerulius
corium
Mycetobiont *
Trametes elegans Mycetobiont * *
Cerioporus mollis Mycetobiont *
Phellinus rimosus Mycetobiont * * *
Fuscoporia
ferruginosa
Mycetobiont *
Trametes sp. Mycetobiont *
Trametes hirta Mycetobiont *
Favolus tenuiculus Mycetobiont *
Pseudofavolus
tenuis
Mycetobiont *
Lentinus crinitus Mycetobiont * *
Heliocybe sulcata Mycetobiont *
Peniophora
quercina
Mycetobiont *
Phellinus gilvus Mycetobiont *
Pluteus cervinus Mycetobiont *
Neofavolus
alveolaris
Mycetobiont *
Pycnoporus
sanguineus
Mycetobiont * * *
Stereum
complicatum
Mycetobiont *
Stereum ostrea Mycetobiont * *
Trametes hirsuta Mycetobiont *
Trametes
occidentalis
Mycetobiont *
Trichaptum
biformis
Mycetobiont *
Family Species Specicity Associated fungi Category 123
Trametes hispida, T. occidentalis, Tremella lutescens, Truncospora ohiensis,
Tulostoma sp. and Xylaria hypoxylon) and at the end of summer with only 7 exclu-
sive species (i.e. Boletus sp., Hygrocybe sp., Mycena margarita, Panaeolina
foenisecii, Phaeocollybia sp., Pluteus longistriatus and Scleroderma citrinum).
Considering the sites for each of the seasons of the year, the MT site had 18 species
of macromycetes in spring, 6 in summer, 13 in autumn and 16 speci es in winter;
the site (BE) recorded 17 species in spring, 12 in summer, 20 in autumn and
16 species in winter; the site (BPE) had 8 species in spring, 11 in summer, 26 in
autumn and 17 species for winter (Fig. 8). In the same way, the number of insect
individuals was recorded for each of the seasons, spring showed the highest value
with 1999 individuals, winter followed with 1029 individuals, autumn ha68
individuals and at the end was summer with 374 individuals of insects (Figs. 9,
10, 11, 12, and 13).
Interactions Between Macrofungi and Insects via Sporocarps in Three... 239
Table 3 (continued)
Sites
Nitulidae Prometopia
sp.
Polyphagy Trametes hirsuta Mycetobiont *
Staphylinidae Phanerota
fascista
Polyphagy Cortinarius sp. Mycetolous *
Armillaria mellea Mycetolous *
Desarmillaria
tabescens
Mycetolous * *
Tenebrionidae Neomida
bicornis
Polyphagy Pycnoporus
sanguineus
Mycetobiont * *
Pycnoporus
sanguneus
Mycetobiont *
Neomida
hemorroidalis
Polyphagy Desarmillaria
tabescens
Mycetobiont *
Stereum ostrea Mycetobiont *
Diaperis sp. Polyphagy Phellinus gilvus Mycetobiont *
Diaperis
rupes
Polyphagy Desarmillaria
tabescens
Mycetobiont *
Annulohypoxylon
thouarsianum
Mycetobiont *
Phellinus gilvus Mycetobiont *
Muscidae Musa
domestica
Polyphagy Lysurus
periphragmoides
Mycetolous *
Ixodidae ND Polyphagy Phavolus
tenuiculus
Mycetoxenic *
Cerioporus mollis Mycetoxenic *
Pseudofavolus
tenuis
Mycetoxenic *
240 E. Rivera-Luna et al.
Fig. 8 Number of insect specimens in fruiting bodies of macromycetes
Fig. 9 Number of macromycetes species at each site per season of the year
Interactions Between Macrofungi and Insects via Sporocarps in Three... 241
Fig. 10 Example of diversity of macrofungal species associated with vegetation types
Fig. 11 Number of insect individuals present in each of the sites by season of the year
242 E. Rivera-Luna et al.
Fig. 12 Main insect species associated to sporocarps in the three localities
Fig. 13 Number of specimens of insects per season
3.5 Data Analysis
A similarity analysis was performed between the sites using the MVSP (Multi-
Variate Statistical Package) using the Sorensen Coefcient, and the results show that
site 2 and 3 (Oak Forest and Oak Pine Forest) have the m value at the top of the
similarity value with 39.2% (IS
S
= 0.392) and these sites are linked by site 1 with TT
vegetation with a similarity value of 18.9% (ISS = 0189). An afnity matrix was
made using the Sørensen Coefcient (Table 4) and the results previously obtained
with the MVSP program, since the highest value occurred between sites 2 and 3 with
a simil arity of 28%, the lowest value was obtained for sites 1 and 3 with a similarity
value of 10%.
Interactions Between Macrofungi and Insects via Sporocarps in Three... 243
Table 4 Afnity matrix with
Sørensen coefcient results
for the collection sites consid-
ering the macromycetes spe-
cies occurring in each of them
Afnity matrix
Site 1
Thorn scrub
Site 2
Oak forest
Site 3
Oak-pine forest
Site 1 0.18 0.10
Site 2 0.82 0.28
Site 3 0.90 0.72
Table 5 Results obtained
using the Shannon-Weiner
Index that determines the
diversity of species at each
sampling site
Diversity in sampling sites
Site 1
Thornscrubs
Site 2
Oak forest
Site 3
Oak-pine forest
2.50 2.55 2.49
Macromycetes species were considered
Using the Shannon-Wiener Index, the three sampling sites were evaluated for the
diversity of macromycetes species present at each site. The result of the index yields
results ranging from 0.5 to 5, being values of 23 as ecosys tems of moderate
diversity, values less than 2 are considered as low diversity and values higher than
3 are ecosystems of high diversity of species.
The results showed that all three sampling sites have a high diversity, the Oak
Pine Forest site had the highest value of the index with 3.59, followed by the Oak
Forest site with 3.57, and at the end the MT site with 3.07. The analysis was applied
in the same way to the species of macromycetes recorded by seasons of the year to
know the diversity that each one had, the results obtained showed that autumn had
the greatest diversity with a value of 3.84, followed by spring with 3.23, winter with
3.13 and summer with 2.90; a value of less than 3 indicates a moderate diversity for
this season of the year (Table 5).
4 Discussion
According to the results of this research carried out in three types of vegetation
located in the municipality of Linares, Nuevo León there is a diversity of
macromycetes of 102 species, they belong to the phylum Ascomycota and
Basidiomycota, the latter had the largest number of species for the three collection
sites.
244 E. Rivera-Luna et al.
Considering the ecological distribution of the identied taxa, the site
(BE) presented 52 species of macromycetes, being the site with the highest number
of recorded species, the sites (MT) and (BPE) had 37 and 46 species respectively.
The largest number of species were collected in the (BE), since it has been reported
that this type of vegetation has the substrate and conditions required for the growth
of most macromycetes species (Pardavé et al. 2013). This is consistent with Pardavé
(1993), Pardavé et al. (2008) and Díaz et al. (2005), who mentioned that many
species of fungi are widely distributed in coniferous, oak and pine forests of Mexico
Insect diversity was present with 4070 individuals of Orders Coleoptera, Hemiptera,
Hymenoptera, Diptera and 2 individuals of the class Arachnida, order Acarina. The
Order Coleoptera had the largest number of individuals in the three vegetation types
sampled with 300 individuals for the TT site, 2075 for the OF site and 1434
individuals for the BPE site. This is consistent with Barraza-Domínguez (2014),
who observed that insects of the Order Coleoptera have a strong association with
macromycetes species.
The association between the species of the two great Kingdoms was analyzed,
observing that the family Polyporaceae recorded 13 species (i.e. Datronia mollis,
Hexagonia hirta, H. papyracea, H. tenuis, Lentinus sulcatus, L. arcularius,
L. crinitus, Polyporus alveolaris, Pycnoporus cinnabarinus., P. sanguineus,
Trametes hirsuta, T. occidentalis and Trichaptum biforme) being the family with
the largest number of species that recorded associations with insect diversity, mainly
with the order Coleoptera. Considering the number of individual insects associated
with each of the macromycete species, the Polyporaceae family has 1950 associated
insects. On the contrary, the insect species with the highest number of associations is
Colenis sp. belonged to the order Coleoptera, this species was present associated as a
mycetobiont with 22 species of macromycetes. Amat (2007) proposed this degree of
association to refer to insects whose associ ation with the fungus is mandatory and
usually depends on it to complete thei r life cycle. Colenis sp., is recorded in the
sporocarps of Antrodia sp., Byssomerulius corium, Daedalea elegans, Datronia
mollis, Fulvifomes rimosus, Fuscoporia ferruginosa, Hexagonia papyracea,
H. hirta, H. hispida, H. tenuis, Lentinus sp., L. crinitus, Peniophora quercina,
Phellinus gilvus, Pluteus cervinus, Polyporus alveolaris, Pycnoporus sanguineus,
Stereum complicatum, Stereum ostrea, Trametes hirsuta,T. occidentalis and
Trichaptum biforme. In the 22 species of macromycetes, galleries were observed
that the Coleorptera formed to feed and deposit their waste. In the case of Lentinus
species, 80% of their sporocarps were used as food by insects, and in some cases up
to 100% of the sporoma was consumed within a period of 30 days. Despite being
registered as a mycetobiont species, its specicity is analyzed as an Olygophagia,
Delgado and Navarrete-Heredia (2011) recognize this level of specicity for insect
species that feed on sporocarps of a few species of macromycetes, and therefore
belong to genera (macromycetes) or closely related genera. The specicity pattern of
Colenis sp. was observed and it was observed that 13 of the 22 species of
macromycetes to which it is associated belong to the Family Polyporaceae, shelf
fungi with soft sporocarps (Hexagonia, Lentinus, Polyporus, Trametes) and hard
sporocarps, for example. (Pycnoporus, Trichaptum), this is consistent with what was
previously mentioned by Delgado and Navarrete-Heredia (2011). The Sorensen
Index was used to observe the similarity of the three collection sites with respect
to the Macromycete species and it was observed that the OF and BPE sites had a
higher similarity index (ISs=0.28), both sites share 28% of the mycobiotic diversity.
On the contrary, we have the MT and BPE sites with a 10% similarity (ISs=0.10).
Considering the height at which the sites are located, in the latter case the altitudinal
difference is 966 m, and Núñez (1996), mentions that, in dissimilarity, height is a
factor very important that inuences the fruiting and formation of basidiospores.
Based on the Shannon index that has been used to observe physical diversity in the
different vegetation types, it was recorded as a result that the three sites have a high
diversity by obtaining the values 3.07, 3.57 and 3.59 respectively.
Interactions Between Macrofungi and Insects via Sporocarps in Three... 245
The results reinforce the proposed hypothesis: There are differences in the
composition and diversity of insect species associated with macromycetes species
in different types of vegetation by season of the year, however, it will be necessary to
make collections for longer periods since the phenology of some species as required,
in addition to covering a larger area in the municipality. The dispersal of spores
through insects is an important process that occurs throughout the year in these
forests. Insect predators may also contribute to the spore dispersal process in the
Halbwachs and Bässler (2015).
5 Conclusions
The results of the research show evidence of a high diversity of insect-fungus
interactions across the sporocarps of macromycetes species in three vegetation
types. The species of fungi involved in these interactions are required for survival
and distribution in each type of vegetation in the municipality of Linares, Nuevo
León. Macromycetes species are distributed in the three types of vegetation based on
ecological or climatic patterns that contribute to their seasonal fruiting. The results of
this research are the rst report of this type of interaction for this locality in Mexico.
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Diccionario de los hongos, 10ª edn
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