Iowa State University Capstones, Theses and Graduate Theses and Dissertations Dissertations
2018 Lichen diversity and conservation of northeast Iowa: White Pine Hollow State Preserve and the lichen Lobaria pulmonaria Kathleen M. Thompson Iowa State University
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Recommended Citation Thompson, Kathleen M., "Lichen diversity and conservation of northeast Iowa: White Pine Hollow State Preserve and the lichen Lobaria pulmonaria" (2018). Graduate Theses and Dissertations. 16677. https://lib.dr.iastate.edu/etd/16677
This Thesis is brought to you for free and open access by the Iowa State University Capstones, Theses and Dissertations at Iowa State University Digital Repository. It has been accepted for inclusion in Graduate Theses and Dissertations by an authorized administrator of Iowa State University Digital Repository. For more information, please contact [email protected]. Lichen diversity and conservation of northeast Iowa: White Pine Hollow State Preserve and the lichen Lobaria pulmonaria
by
Kathleen Marie Thompson
A thesis submitted to the graduate faculty
in partial fulfillment of the requirements for the degree of
MASTER OF SCIENCE
Major: Ecology and Evolutionary Biology
Program of Study Committee: James T. Colbert, Major Professor Haldre Rogers Leonor Leandro
The student author, whose presentation of the scholarship herein was approved by the program of study committee, is solely responsible for the content of this thesis. The Graduate College will ensure this thesis is globally accessible and will not permit alterations after a degree is conferred.
Iowa State University
Ames, Iowa
2018
Copyright © Kathleen M. Thompson, 2018. All rights reserved. ii
DEDICATION
This thesis is dedicated, in part, to my two nieces, Mila and Lanie Ruge. I hope your curiosity and enthusiasm never cease and you recognize that you can do whatever, and be whomever, you wish. I have very much enjoyed watching you two grow up thus far, and I could not be more excited to see who you will become. The world is yours.
This thesis is also dedicated to Dr. Lois H. Tiffany, who was a mycologist and educator at Iowa State University for more than 50 years. As a female scientist in the mid
1900s, Dr. Tiffany faced overt sexism and discrimination. Nevertheless, she was persistent, and after initially being offered no pay for her faculty position in the Iowa
State Botany Department in 1950, she achieved the status of “Full Professor” in 1965 and served as the chair of the department from 1990 to 1996. Among other honors, she became the first female president of the Iowa Academy of Science in 1977 and was the first woman to be deemed a “Distinguished Professor” in the College of Liberal Arts and
Sciences at Iowa State in 1994. Dr. Tiffany published more than 100 scientific papers, as well as a handful of books, and has been considered to be the "Renaissance woman of mycological research".
Dr. Tiffany was responsible for engaging my advisor, Dr. Colbert’s, interest in fungi, which supported his interest in lichens. Dr. Colbert introduced me to my fascination with lichens, which paved the way for my interest in fungi. In this sense, I consider Dr. Tiffany to be my “mycological grandmother”. Though I unfortunately never had the opportunity to meet her, I think it is safe to say we would have gotten along quite well. I hope to someday be a similar source of inspiration and symbol of perseverance to females – including my nieces – and other scientists, just as she has for me. iii
TABLE OF CONTENTS
Page
LIST OF FIGURES ...... iv
LIST OF TABLES ...... v
ACKNOWLEDGMENTS ...... vi
ABSTRACT ...... viii
CHAPTER 1. GENERAL INTRODUCTION ...... 1 The Symbiosis ...... 1 The Mutualism ...... 4 Lichen Morphology and Reproduction...... 6 Lichen Ecology ...... 9 Conservation of Lichens ...... 14 Literature Cited ...... 19
CHAPTER 2. LICHENS OF WHITE PINE HOLLOW STATE PRESERVE ...... 27 Abstract ...... 27 Introduction ...... 27 Area of Study ...... 28 Methods ...... 32 Results...... 34 Discussion ...... 35 Literature Cited ...... 41 Tables ...... 45 Figures ...... 55
CHAPTER 3. ASSESSING THE REINTRODUCTION POTENTIAL OF THE NATIVE IOWA LICHEN LOBARIA PULMONARIA ...... 57 Abstract ...... 57 Introduction ...... 57 Methods ...... 63 Results...... 67 Discussion ...... 67 Literature Cited ...... 69 Figures ...... 74
GENERAL CONCLUSION ...... 77 iv
LIST OF FIGURES
Page
Figure 2.1 Map illustrating past disturbances in White Pine Hollow State Preserve in Dubuque County, Iowa, including the prevalence of logging. Adapted from the White Pine Hollow State Preserve Ecological Management Plan (Johnson 2000)...... 55
Figure 2.2 Map showing location of collections made at White Pine Hollow State Preserve, Dubuque County, Iowa. The size of the point correlates with the number of collections made at each particular location...... 56
Figure 3.1 Map of the replicate boards showing the randomization of the eight treatments, including those on bark from White Pine Hollow (WPH) and Chippewa National Forest (CNF). This representation is photo- documented in Figure 3.2...... 74
Figure 3.2 Lobaria pulmonaria reintroduction simulation set-up. Each of the eight boards contained a representative of each of the eight treatments (see Figure 3.1)...... 75
Figure 3.3 Treatment squares containing asexual propagules (left), young thalline lobes (center), and adult thalli (right)...... 76 v
LIST OF TABLES
Page
Table 2.1 Lichens of White Pine Hollow State Preserve (WPH) reported previously to the CNALH (accessed February 19th, 2018) or observed during this study. Names were updated to Esslinger 2018 (accessed February 12th, 2018). *Deprecated name, but varieties not specified...... 45
Table 2.2 Complete list of lichens collected on algific talus slopes, as well as the percentage of collections of each distinct lichen made on the algific talus slopes. Species in bold print are newly reported for the State of Iowa...... 53
vi
ACKNOWLEDGMENTS
This work could not have been completed without the assistance and support of a number of people and organizations. First and foremost, I extend an immeasurable amount of gratitude to my advisor, Dr. Jim Colbert. Not only did he open my eyes to the wondrous world of lichens as an undergraduate, but he also served as the most dedicated and supportive mentor a graduate student could hope for. I could not be more appreciative of the time and energy he spent fostering my development as a scientist, educator, and individual, and I hope to be half the mentor he has been for me to any future students I am fortunate enough to advise.
I would also like to especially acknowledge and thank the additional members of my committee. Dr. Leonor Leandro furthered my interest in and knowledge of fungi and
Dr. Haldre Rogers was instrumental in the development of my future plans. I am forever grateful for their contributions.
In addition, I thank John Pearson of the Iowa Department of Natural Resources for permission to collect at White Pine Hollow State Preserve and for his endless insight.
I also thank Deborah Lewis of the Ada Hayden Herbarium for providing lab space, equipment for lichen identification, and infinite enthusiasm. A number of these identifications could not have been made without the very generous assistance of Caleb
Morse of the R.L. McGregor Herbarium at the University of Kansas and James Lendemer of the New York Botanical Garden. I also thank Bobby Henderson with the Minnesota
Department of Natural Resources for permission to collect propagation material of the lichen Lobaria pulmonaria. Workshop instruction provided by Irwin Brodo, David vii
Richardson, Mark Seaward, and Taylor Quedensley was incredibly valuable in establishing a broad knowledge of lichen natural history and identification techniques.
Sources of funding for this research included the Culberson and Hale Award for
Lichenological Research from the American Bryological and Lichenological Society and the Lois H. Tiffany Scholarship Award from Iowa State University; the generous contributions from both institutions is very much appreciated. Special acknowledgments go out to Hannah Carroll for her statistical programming expertise, Steve Mahoney and
Kenneth McCabe for providing assistance with and greenhouse space for the lichen propagation experiment, and DeWitt Boyd and Amy Podaril for their involvement in lichen collection.
Most importantly, I wish to thank my family for their endless and unwavering support. They continue to provide me with guidance, love, and encouragement in all that
I pursue, and I could not be more fortunate to have them, as well as everyone else mentioned above, in my life. viii
ABSTRACT
A lichen diversity survey of White Pine Hollow State Preserve in Dubuque
County, Iowa, was conducted. The study revealed the presence of 117 different lichens, which, when combined with previous records, leads to a total of 147 lichens reported for the preserve. The lichens observed in this study included 13 previously unreported lichens for the State of Iowa and three reported on only one prior occasion. This increases the number of lichens reported for the State of Iowa to a total of 478 from the previous estimate of 465.
The lichen Lobaria pulmonaria (L.) Hoffm. was not amongst the lichens observed, although White Pine Hollow was the location of one of the last known collections of this lichen in Iowa. Lobaria pulmonaria is an old-growth specialist that suffered major declines throughout the 1900s and is currently decreasing in North
America – including its range in northeast Iowa. Efforts were made to propagate L. pulmonaria in a greenhouse setting as a means of providing insight to whether a reintroduction of this lichen to its historic range in Iowa might be feasible. Asexual propagules, including soredia and isidia, and young thalline lobes were applied to bark from White Pine Hollow and monitored for 12 months under greenhouse conditions. At the conclusion of the study, no growth had occurred in any of the treatments. Given the lack of growth in treatments on the control substrate and worsening condition of the adult thallus controls, it is likely that the unsuccessful result of this study is due to procedural aspects or greenhouse conditions as opposed to an incompatibility of L. pulmonaria with bark from White Pine Hollow. The difficulty in propagating L. pulmonaria under ix controlled conditions emphasizes the need for greater protection efforts for this lichen, as well as others, in locations where they remain present.
1
CHAPTER 1. GENERAL INTRODUCTION
“There is a low mist in the woods—
It is a good day to study lichens.”
Henry David Thoreau, 1851
The Symbiosis
Although commonly regarded as “just plants” when noticed at all by members of the general public, lichens are both wonderful components of our planet’s biological diversity and quite distinct from members of Kingdom Plantae. Present on Earth as early as 600 million years ago (Yuan et al. 2005) and found in virtually every terrestrial habitat, lichens are evolutionarily ancient and extremely successful symbiotic associations. They consist primarily of fungal and photosynthetic components, which are often referred to as mycobionts and photobionts, respectively. The traditional definition of a lichen has long emphasized this duality in the relationship between mycobiont and photobiont, but recent studies (Paulsrud 1999, Liba et al. 2006, Honegger 2008, Grube et al. 2009, Bates et al. 2011,
Casano et al. 2011, Spribille et al. 2016) have revealed a much greater level of complexity.
Approximately 85% of mycobionts are associated with green algae and 10% with cyanobacteria; the remaining 3-4% of lichens include both types of photobionts in the lichen thallus, or vegetative body (Honegger 2008). These are referred to as tripartite – as opposed to bipartite – lichens. In the vast majority of tripartite lichens, the cyanobacterium is contained in gall-like structures known as cephalodia. There are exceptions, however, such as the lichen Euopsis granatina (Sommerf.) Nyl., which houses both the green algal and cyanobacterial components throughout the lichen thallus (Büdel and Henssen 1988, as cited 2 in Nash 2008a), as well as Muhria urceolata P. M. Jørg., which has a layer of algae atop a filamentous mat of cyanobacteria (Jørgensen and Jahns 1987). There are even mycobionts that exhibit a particular morphology when associated with green algae and a completely different one when associated with cyanobacteria, such as the lichens Lobaria amplissima
(Scop.) Forssell (green alga) and Dendriscocaulon umhausense (Auersw.) Degel.
(cyanobacterium). These different forms are described as photosymbiodemes, photomorph pairs, or morphotype pairs and imply that a substantial portion of lichen morphology is due to the influence of the photobiont (Honegger 2008).
Photosymbiodemes not only challenge the conventional notion of a specific mycobiont requiring a specific photobiont, but they complicate traditional lichen taxonomy, which designates the scientific name of the symbiosis as that of the fungal partner. It has been proposed that some sort of informal naming system should be developed to handle such situations for increased practicality (Jørgensen 1998). However, this begs the question: are traditionally used species delimitations applicable to – and useful for – lichen taxonomy? It also highlights how much more there may be to discover regarding phenotypic plasticity in lichenized fungi.
In addition to tripartite lichens and photosymbiodemes, there is also evidence that multiple species of either green algae or cyanobacteria can occur within the same thallus of a seemingly “bipartite” lichen (Casano et al. 2011, Paulsrud 1999, Nash 2008a). It would be interesting to learn how photobiont diversity affects the overall symbiosis and whether there is a general trend toward competition or coexistence – particularly between closely-related photobionts. 3
Despite the concept of duality and partner specificity being challenged from the perspective of the photobiont, it was not until very recently that this concept was questioned with regard to the mycobiont. For the past 140 years, there was thought to be only one species of fungus present in each lichen – with the exception of an occasional parasitic or endolichenic fungus (Richardson 1999, U’Ren et al. 2010). In fact, as previously mentioned, the scientific name of each lichen is considered to be that of the fungal partner. The vast majority of traditional lichen mycobionts belong to the Phylum Ascomycota (~99%), though some belong to the Phylum Basidiomycota (~1%) (Honegger 2012). With many different and distantly related fungi able to form lichens, it has been demonstrated that the ability to lichenize is a result of convergent evolution instead of evolution from a common lichen ancestor (Brodo et al. 2001). It has been estimated that 14 to 23 lineages of ascomycetes and
6 to 7 lineages of basidiomycetes have lichenized members, though the majority of known lichens are members of just 9 lineages of ascomycete fungi (Lücking 2016).
In 2016, however, a groundbreaking study was published revealing the presence of a secondary mycobiont in the majority of lichens assessed: a basidiomycete yeast (genus
Cyphobasidium; Spribille et al. 2016). These yeasts were found to be specific to particular lichen associations as well as shed light on phenotypic variations that were previously inexplicable. Furthermore, given its high concentration in the upper cortex, or the stratified layer of the thallus furthest from the substrate, it is thought that this yeast not only plays a critical role in the formation of this important structural feature, but it may also explain why the reconstruction of lichens in vitro has been so challenging and often results in rudimentary cortex formation (Spribille et al. 2016). Perhaps of most interest is the suggested relationship 4 between this additional mycobiont and the evolutionary radiation and diversification of major lineages of certain macrolichens (Spribille et al. 2016).
The presence – and importance – of diverse bacterial communities within lichen thalli is also gaining attention. These assemblies are suspected to help with the acquisition of nutrients such as nitrogen, phosphorus, and amino acids and have also been found to be distinct between species (Bates et al. 2011, Liba et al. 2006, Grube et al. 2009). Although the concept of a seemingly distinct organism being comprised of many species is not new (e.g., humans and their gastrointestinal microbial communities; Human Microbiome Project
Consortium 2012), the previously emphasized duality of the single mycobiont – single photobiont association is most certainly oversimplified and may, in fact, extend beyond the mycobiont(s) and photobiont(s) altogether.
The Mutualism
Lichens have long been the poster children for mutualistic relationships despite there being little experimental evidence supporting this type of interaction (Ahmadjian and Jacobs
2011, Richardson 1999). The primary argument supporting the lichen mutualism is that although most of the photobionts found within lichens can live freely (as opposed to the mycobionts), in a lichenized state they are able to grow in habitats in which they would not normally be able to survive. This includes habitats such as exposed surfaces with higher levels of UV radiation than they could tolerate independently as well as an increased chance of desiccation (Kranner et al. 2008, Gauslaa and Solhaug 2001, Honegger 1993). In fact, not only can the lichen association tolerate some of the toughest extremes on Planet Earth, some can also withstand the brutal conditions of outer space (Sancho et al. 2007, Raggio et al.
2011). 5
Conversely, there is a body of evidence supporting a controlled parasitism
(Ahmadjian and Jacobs 2011, Richardson 1999, Ahmadjian 1993, Ahmadjian and Jacobs
1981, Kershaw and Millbank 1970). Evidence for the controlled parasitism includes the allocation of photosynthetic products of the photobiont to the fungus via haustoria (the same apparatus used by plant pathogenic fungi), the presence of dead algal cells, control of the photosynthetic rate of the photobiont by the mycobiont, fungal regulation of photobiont access to water and nutrients, fungal control of the size, rate of growth, and reproductive capacity of the photobiont, and that we have yet to find lichen-forming fungi living freely in the wild (Richardson 1999, Nash 2008a, Zoller and Lutzoni 2003, Kranner and Beckett 1998,
Ahmadjian 1993, Honegger 1993). Furthermore, it has been long thought that fungal melanins and compounds producing coloration serve as a source of UV protection for the sensitive photobionts (Gauslaa and Solhaug 2001, Karunaratne 1999, Solhaug and Gauslaa
1996). A recent study, however, demonstrated that the fungal hyphae in certain lichens are actually more sensitive to high levels of UV radiation than their algal counterparts
(Chowdhury et al. 2017).
With evidence suggesting more than one state of the interaction, the true nature of the symbiosis continues to be debated (Nash 2008a). Lichens may exhibit a context-dependent interaction, ranging from mutualistic to parasitic, that varies over time and space and is influenced by associated biotic and abiotic factors. A similar situation exists in mycorrhizal as well as ant-plant interactions (Hoeksema and Bruna 2015, Chamberlain and Holland
2009). There is likely still much to learn regarding the plasticity of mycobiont and photobiont interactions, as well as those with associated bacterial communities, and how this interaction plasticity may influence the overall phenotypic plasticity of the lichen. 6
Lichen Morphology and Reproduction
Lichens are often broadly categorized into three major growth forms: crustose, foliose, and fruticose. Crustose lichens form a tightly-appressed, crust-like growth on the surface of the substrate and possess an upper cortex, but lack a lower cortex – or layer of tightly-woven, conglutinate fungal hyphae. Lichens exhibiting a foliose growth form are characterized by a leaf-like appearance with flattened lobes that contain both upper and lower cortices. Fruticose lichens are defined by being three-dimensional, often shrubby or pendant, with a common cortex that covers the outer surface area.
There are also intermediate forms that may share characteristics of more than one major growth form. Squamulose lichens, for example, are composed of small, foliose- looking fragments or scales that often overlap. They can be tightly-appressed to the substrate or ascending and, therefore, fall between the foliose and crustose growth forms. Leprose lichens, on the other hand, are comprised almost entirely of propagules containing fungal hyphae and green algal cells (soredia), giving them a powdery or cottony appearance.
Leprose lichens lack an upper and lower cortex altogether.
The portion of the lichen that takes on the aforementioned growth forms is referred to as the thallus. This is the main, vegetative body of the lichen that houses the photobiont(s) as well as any additional bacterial and fungal species present in the symbiosis. Lichen thalli are composed primarily of fungal tissue and can be either stratified (heteromerous) or non- stratified (homoiomerous) internally. Those that are stratified often contain four major layers: upper cortex, photobiont layer, medulla, and lower cortex.
The upper cortex is composed of tightly-woven, conglutinate fungal hyphae and houses the recently discovered third major component in the lichen symbiosis – the 7 basidiomycete yeast (Spribille et al. 2016). It is often pigmented by the presence of various chemical compounds, such as usnic acid (yellow to green), vulpinic acid (chartreuse), parietin (orange), or certain xanthones (yellow to brown; Karunaratne 1999). The resulting coloration has long been thought to play a role in UV protection of the photobiont
(Karunaratne 1999, Solhaug and Gauslaa 1996). However, with the recent finding that mycobionts may, in fact, be more sensitive to UV radiation than their photobiont counterparts (Chowdhury et al. 2016), it is currently unclear which partner these pigments actually serve to protect.
In stratified lichens, the photobiont layer lies below the upper cortex and includes either green algal or cyanobacterial cells. This appears to be a rather effective strategy for harvesting light energy, as a similar arrangement can be seen in the organization of palisade parenchyma cells in C3 plant leaves (Esau 1977). Under the photobiont layer lies the medulla, which is a layer of loosely interwoven fungal hyphae with a large amount of intercellular airspaces that are thought to play a role in gas exchange (Honegger 1991, 1993).
Below the medulla lies the lower cortex, which, similar to the upper cortex, is a layer of conglutinate fungal hyphae that subtends the lichen thallus. In foliose lichens, this layer often has projections known as rhizines that function to anchor the lichen to its substrate.
Non-stratified lichens differ in their lack of a distinct photobiont layer and medulla.
Instead, the photobiont component is distributed throughout the internal portion of the thallus. This is common in cyanolichens, or lichens containing cyanobacteria as their photobiont, which often take on a gelatinous texture when hydrated. For this reason, they are often referred to as jelly lichens. 8
Lichen thalli are capable of producing various structures involved in asexual reproduction. Certain lichens, such as those in the genera Usnea, Bryoria, Ramalina, and
Alectoria reproduce primarily via vegetative fragmentation (McCune and Geiser 2009).
Many lichens, however, produce structures specifically for the purpose of asexual reproduction, with the two most common being isidia and soredia. Both isidia and soredia contain fungal hyphae from the mycobiont as well as photobiont cells – and perhaps the associated basidiomycete yeast and bacterial communities, though no confirming studies have been published at this time. These propagules can be produced in relatively large quantities and contain most (if not all) partners necessary to produce a genetically identical thallus. Dispersal of these propagules can occur via physical forces, such as wind, but can also occur through the activities of animals, such as insects.
Although the lichen symbiosis itself cannot reproduce sexually, the mycobiont of many lichens is capable of sexual reproduction. The spores produced through meiosis by the mycobiont (typically ascospores) contain only the genetic information of the fungal partner.
Therefore, not only does each spore need to be distributed to a suitable habitat, but it also needs to acquire the appropriate photobiont(s), basidiomycete yeast, and any important bacterial communities to be successful. This is similarly true for lichens that produce structures known as pycnidia, which produce asexual spores called conidia. Conidia also contain only the genetic information of the mycobiont, and, as products of mitosis, are all genetically identical for any individual lichen. The low probability of success in sexual reproduction may explain why a significant number of lichens reproduce asexually (Tripp
2016, Bowler and Rundel 1975), including some that rely exclusively on asexual reproduction, such as those in the genus Lepraria (Lendemer and Hodkinson 2013). 9
However, fungal spores are much lighter in weight than asexual propagules, such as isidia and soredia, and are therefore less limited in regards to their long distance dispersal ability
(Pentecost 1981, Scheidegger and Werth 2009).
Specialized reproductive structures, referred to generally as either ascomata or basidiomata depending on the phylum of the mycobiont, are responsible for producing ascospores or basidiospores, respectively. Most lichenized fungi produce ascomata, which can be further divided into particular types – such as apothecia and perithecia. Apothecia look like discs or saucers and are characterized by having an exposed hymenium, or spore- producing layer. Perithecia, on the other hand, have an enclosed hymenium and are pear- shaped in appearance, with a small opening called an ostiole at the summit. The characteristics of these reproductive structures, as well as associated spores, are crucial for proper identification in a large number of lichens.
Lichen Ecology
Lichens are distinctive in their ability to colonize virtually every terrestrial substrate in regions ranging from artic to tropical, with some having very widespread distributions (i.e,
Cetraria aculeate (Schreber) Fr., Fernańdez-Mendoza et al. 2011) and some exhibiting varying levels of endemism (i.e., Willeya diffractella (Nyl.) Müll. Arg., Gueidan and
Lendemer 2015; Pseudocyphellaria rainierensis Imshaug, Sillet and Goward 1998).
Common substrates for lichen growth include rock, bark, and wood, with these lichens referred to as saxicolous, corticolous, and lignicolous, respectively. However, additional lichen substrates include – though are not limited to – bone, shell, leaves, soil, bryophytes, and human-made substrates such as cement, metal, glass, plastic, and fabric. Certain lichens exhibit a high level of substrate specificity, such as Phaeocalicium curtisii (Tuck.) Tibell, 10 which is restricted to Rhus typhina L. (Brodo 1973) and potentially spatially restricted to the bases of dead main branches of this species (Selva 1988, Nash et al. 2004). Other lichens, however, are much more general with regard to their substrate preferences, including the lichen Lepraria finkii (B. de Lesd.) R.C. Harris, which can grow on rock, soil, bark, and bryophytes.
Due to their ability to grow on rock and photosynthesize, lichens are some of the initial “pioneering” species that move into an area after major disturbances, such as volcanic eruptions, severe fires, and after glacial retreat (Brodo et al. 2001, Raggio et al. 2012, Garty and Binyamini 1990, Cooper 1953, Jackson 1971). Lichens, therefore, play an instrumental role in primary succession and have been shown to be effective in the biodeterioration of rock surfaces (Seaward 2008). Their pedogenetic, or soil-forming, abilities are the result of both chemical and physical processes carried out by the release of chemical compounds, such as oxalic acid, as well as the penetration and permeation of fungal hyphae into and throughout the rock substrate (Seaward 2008). Furthermore, lichens readily accumulate nutrients such as phosphorous, nitrogen, and sulfur from the environment, and, therefore, provide nutrients as well as substrate to successive organisms (Seaward 2008).
Lichens are also ecologically important through their ability to fix carbon and nitrogen. Though one may predict their contribution to be insignificant due to their small size, the ability of lichens to grow on substrates and in habitats where vascular plants cannot results in a large amount of terrestrial surface area covered by lichens. Cyanolichens, or those containing a cyanobacterial photobiont, have the ability to convert atmospheric nitrogen to forms useable by plants and animals through a process called nitrogen fixation. This
“useable” nitrogen, in the form of ammonia or nitrates, can be leached from the lichen thallus 11 or made available to surrounding organisms when the lichen dies. In certain ecosystems, it has been estimated that as much as 50% of the nitrogen input is from lichens (Elbert et al.
2012, Brodo et al. 2001). This, in turn, supports plant communities and creates a positive feedback loop with regard to carbon sequestration (Elbert et al. 2012). Lichens are distinctive in their ability to play a role in both intra- as well as intersystem nutrient and mineral cycles.
With their capability to intercept nutrients from atmospheric and rainfall sources, lichens can incorporate nutrients from outside of the ecosystem that would normally be lost or unable to be utilized. This has important implications, particularly for nutrient-poor systems (Nash
2008b, McCune and Geiser 2009).
In additional to nutrient cycles, lichens also play a key role in the hydrologic cycles of particular habitats by increasing water storage capacity and modulating humidity (Pypker et al. 2006). In fact, the three-dimensional structure of certain lichens has been shown to reduce the amount of water lost by raindrop splashes and prevent runoff from tree branches (Pypker et al. 2006). Furthermore, lichens intercept and reduce the loss of moisture in arid and semi- arid habitats – where access to water is crucial – through the formation of biotic soil crusts.
These soil crusts play an important role in soil stabilization, act as a source of carbon and nitrogen, provide micronutrients to established vegetative communities, and can help favor the survival of native as opposed to invasive plant species (Root et al. 2011; Belnap and
Gillette 1998).
There are many ecological interactions between lichens and animals. The lichen
Cladonia rangiferina (L.) F. H. Wigg. is the primary food source for the caribou (Rangifer tarandus L.), comprising 90% of their winter diet and 50% of their summer diet (Brodo et al.
2001). Caribou are currently classified as a “Vulnerable” species by the International Union 12 for Conservation of Nature (IUCN) and population numbers are declining around the world
(IUCN 2018). The only remaining caribou population in the contiguous US is down to 11 individuals. Currently, lichens are being collected to feed pregnant does in an attempt to increase the population’s size (Schwing 2018). However, many other large animals such as moose, elk, mule deer, black- and white-tailed deer, bighorn sheep, mountain goats, and pronghorn antelope use lichens as a food source, and sometimes as an important survival food (Brodo et al. 2001). Small mammals such as the northern flying squirrels (93% of winter diet and 80% of summer diet, Brodo et al. 2001), red-backed voles, chipmunks, pikas, and mice consume lichens as well (Brodo et al. 2001, McCune and Geiser 2009). Certain lichen species are also utilized as nesting materials for as many as 45 North American bird species, various species of bats and squirrels, as well as pikas and rodents (McCune and
Geiser 2009). Furthermore, a number of invertebrates and arthropods utilize lichens as habitat, nutrition, or mimic them for camouflage, such as larval stage of lacewing insects
(Chrysopidae) and various species of moths (Brodo et al. 2001, McCune and Geiser 2009).
In addition to their ecological roles, lichens have also proven themselves as useful tools for ecological research. Certain lichens are thought to be indicative of specific habitats worthy of conservation (Tibell 1992). In the practice of retention forestry, the presence of certain lichens is used to determine which trees will be left standing as a means to promote biodiversity and create a habitat more similar to one that has undergone natural disturbances as opposed to logging (Perhans et al. 2014). Lichen communities tend to change as their habitat vegetation changes, as shown in a study comparing lichens present in old-growth forests to those in second-growth forest (Lesica et al. 1991). This relationship allows lichens to be useful as indicators of plant succession and habitat continuity (Tibell 1992). In addition, 13 lichens are indicative of microhabitat and microclimate distributions as well as biodiversity hotspots (McCune and Geiser 2009).
Another common and important use of lichens in ecological research is as bioindicators of air quality. Lichens are particularly sensitive to environmental pollutants due to their anatomy and physiology, as well as their sessile nature. In order for a lichen to function properly, the health of the mycobiont and photobiont must be maintained. If this balance is disrupted, due to the presence of a pollutant, for example, the symbiosis can be interrupted, and the lichen may begin to senesce. In general, lichens are sensitive to a number of different air pollutants: sulfur dioxide, ammonia, sulfuric and nitric acids, fluorine, ozone, hydrocarbons, as well as various metals such as lead, copper, zinc, cadmium, and chromium
(Goyal and Seaward 1982, McCune and Geiser 2009, Brodo et al. 2001). Photobionts tend to be particularly vulnerable to pollutants as a consequence of their ability to oxidize photosynthetic pigments as well as alter enzyme activity and compromise cellular and membrane structure and integrity (Paoli et al. 2010, Brodo et al. 2001, McCune and Geiser
2009). Lichens are highly efficient at accumulating atmospheric toxins and pollutants in their thalli. They tend to accrue these pollutants in proportion to their presence in the surrounding environment, making them useful in constructing pollution gradients with regard to space and time (McCune and Geiser 2009).
Lichens have been used as monitors of air quality near industrialized regions (Geiser and Neitlich 2007), including coal-fired power plants (Showman 1975), as well as agricultural regions (Podaril and Colbert 2016, Ruisi et al. 2005, Geiser and Neitlich 2007).
They have also been used to indicate the presence of acid rain (Gilbert 1986) and depict climatic gradients (Geiser and Neitlich 2007) that could potentially be used to track climate 14 change. In addition, their sensitivity and response to poor air quality provides evidence of the environmental harm caused by atmospheric pollutants as well as suggests the possibility of larger effects on ecosystems and their functioning (McCune and Geiser 2009).
In addition to their utility as monitors of air quality, lichens have also shown to be useful as indicators of water quality. A concentration gradient of toxic metals was constructed near an industrial drainage in the Bayou d’Inde in Louisiana using PVC pipe apparatuses filled with the lichen Parmotrema praesorediosum (Nyl.) Hale (Beck and
Ramelow 1990). Furthermore, the ability of lichens to readily absorb and accumulate metals from aqueous solutions suggests a practical alternative for the treatment of industrial wastewater, as demonstrated with the lichen Cladonia rangiformis Hoffm. (Ekmekyapar et al. 2006).
Conservation of Lichens
The science of conservation biology was developed as a response to the loss of biodiversity across the globe, commonly as the result of human activities (Van Dyke 2010).
In the words of John Muir: “When we try to pick out anything by itself we find that it is bound fast by a thousand invisible cords that cannot be broken, to everything in the universe”
(as cited in Hatch 2012). Being a poorly-studied group of organisms by comparison to other taxa, we may be losing more than we realize with the disappearance of particular lichens.
Lichens are rarely considered as targets for conservation. There is currently only one lichen (Cetradonia lineare [Evans] J. C. Wei & Ahti) included on the United States Fish and
Wildlife Service’s list of Threatened and Endangered Species, with another (Phaeophyscia leana [Tuck.] Essl.) under consideration (Fish and Wildlife Service 2018), and thirteen on the
IUCN’s Red List of Threatened Species (Anzia centrifuga Haugan., Buellia asterella Poelt & 15
Sulzer, Caloplaca rinodinae-albae Poelt & Nimis, Cetradonia linearis [A.Evans] J.C.Wei &
Ahti, Cladonia perforate A. Evans, Erioderma pedicellatum [Hue] Jørg., Everniastrum nepalense [Taylor] Hale ex Sipman, Gymnoderma insulare Yoshim. & Sharp, Leptogium rivulare [Ach.] Mont., Phaeophyscia hispidula [Ach.] Essl., Ramalina erosa Krog, Ramalina timdaliana Krog, Sticta alpinotropica Aptroot; IUCN 2018). This limited number, however, is more likely due to limited data than to very few lichens being threatened, endangered, or extinct.
The general disregard of lichens – particularly on the conservation agenda – is an unfortunate consequence of being difficult to find and identify, which is linked to the lack of diversity and distribution records. Being sensitive to many of the changes taking place in our human-impacted environment and often having specific substrate and habitat requirements, the conservation of lichens is a topic that needs to be addressed – and promptly. The lichen symbiosis, however, presents a number of unique challenges with regard to conservation, requiring a nontraditional perspective on how to approach their protection. One of these challenges is how we define a lichen “species”.
Most conservation strategies are aimed at preserving and protecting biodiversity from extinction – with “species” serving as the basic units of biodiversity. How species are defined, therefore, is important with regard to their conservation. In the words of conservation biologist Fred Van Dyke, “Our definition and understanding of what a species is affects how we will manage and conserve it” (Van Dyke 2010). As previously mentioned, lichens are the result of an interaction between multiple partners – further convoluting their categorization. It would seem appropriate to define lichen management plans based on all associated partners, however, the mycobiont is generally the sole target (Scheidegger and 16
Goward 2002). This seems to come back to the words of Van Dyke: lichens are named after the primary fungal component of the symbiosis and the conservation and management strategies for lichens are defined from the perspective of this partner. Having relatively recently discovered the amount of biological diversity present in each lichen thallus, as well as the level of importance these constituents play in the overall interaction, we may be misinterpreting the best way to conserve rare or endangered lichen symbioses due to our own bias.
The range of a particular lichen depends on both the availability of the mycobiont as well as that of the photobiont and all other necessary partners. In order to properly manage for lichens, it may be necessary to know which constituents are present as well as their individual distributions. It has been demonstrated that lichen photobionts exhibit preferences for certain environmental characteristics that may, ultimately, limit the niche space available to certain lichens (Peksa and Škaloud 2011). There is currently little information available on the distribution of various photosynthetic partners – which is not surprising. In order to accurately identify most lichenized photobionts, even to the genus level, they must be isolated and grown in culture (Brodo et al. 2001, McCune and Geiser 2009). This explains why only ~2-3% of lichen photobionts have been identified at the species level (Brodo et al.
2001). Furthermore, there are algal partners that have yet to be found outside of the lichenized state, making their free-living distribution maps impossible to create (Brodo et al.
2001). This information would be of particular importance for those species that reproduce primarily via sexual or asexual spores.
An increasing amount of attention has been given to the conservation of biological interactions as opposed to solely a species-scale consideration (Winfree et al. 2015). Included 17 in this field is the conservation and restoration of mutualistic relationships, including symbioses such as corals and dinoflagellates, figs and fig wasps, plants and mycorrhizal fungi, ants and plants, and plants and endophytic fungi (Berkelmans and van Oppen 2006,
McKey 1989, Richter and Stutz 2002, Korb et al. 2003, Wilson et al. 2009, Rickson and
Rickson 1998, Iqbal et al. 2012). As mentioned, mycobionts are currently the sole target of lichen conservation programs (Scheidegger and Goward 2002). However, as the lichen symbiosis continues to become better understood, including the role of all partners involved, it is possible that this approach will also be useful in the conservation of lichens.
Lichens should, additionally, be considered differently than other taxa when assessing their vulnerability as a result of their inherent anatomy and physiology. Devoid of roots, waxy cuticles, vascular tissue, and stomata with guard cells – as found in most of their botanical counterparts – lichens uptake water and nutrients directly from the atmosphere
(Nash 2008b). Photobionts require moisture to photosynthesize; however, a hydrated thallus allows the deposition and passive absorption of gaseous and finely particulate pollutants
(McCune and Geiser 2009). Although passive diffusion requires little to no extra energy expenditure, lichens have essentially no way of discerning what is and is not permitted to enter the thallus. Furthermore, atmospheric sources of moisture, such as fog or dew, tend to be more highly concentrated with regard to pollutants, and the ability of lichens to survive periods of dehydration result in a further concentration of contaminants (Nash 2008b).
Lichens also lack internal tissues and deciduous structures that are able to compartmentalize, process, and/or reduce the accumulation of toxins (Nash 2008b, McCune and Geiser 2009).
The additive effect of the aforementioned characteristics makes lichens particularly susceptible to harmful contaminants that are present in the surrounding environment. 18
An additional confounding factor with regard to the conservation of lichens is a result of their general imperceptibility and difficulty in accurate identification. Lichens tend to be small and slow growing. Even some of the fastest growing species can only add up to two centimeters radially (Peltigera sp.) or increase their overall mass by 33.3% (Ramalina menziesii, Lobaria oregana) each year (Brodo et al. 2001). Furthermore, many lichens often look quite similar to their substrate. In short: many lichens can be difficult to find and notice
– especially those that grow in tiny nooks of rocks or high in the canopies of old trees. In addition to the difficultly of finding them, identifying lichens – and doing so accurately – is an even greater challenge. Although some lichens can be identified in the field with experience and, perhaps, a hand lens, the vast majority require the use of dissecting and compound microscopes, extensive dichotomous keys, chemical tests, and often the presence of distinguishing features or reproductive structures in order to identify the specimen to the
“species”, or even genus, level. Unfortunately, if one or more of these key features or structures is missing or underdeveloped, the resulting identification may not be accurate – or possible. It also often takes an expert who has developed a well-trained eye to distinguish and interpret the minuscule features that characterize one particular lichen from another. The increased taxonomic complexity revealed by molecular data makes the task of morphological identification even more challenging.
Given the difficulty involved in locating and identifying lichens, it is not at all surprising that past diversity and distribution records of lichens are limited or lacking. An additional cause for the paucity of historic lichen records is their low level of appreciation throughout history. Even the famous Carolus Linneaus referred to lichens as “rustici pauperrimi”, or “the poor trash of vegetation” (Johnson and Villella 2013; Walewski 2007). 19
Iowa has historically been no exception to this sentiment. As of 2015, 44 of Iowa’s 99 counties had less than 10 reported lichen accessions, or formally collected specimens, with
39% of these being made prior to the year 1960 (Podaril and Colbert 2015). The significance of these numbers, with regard to lichen conservation, is that Iowa, and the many other states who fail to have current and comprehensive records of their lichen diversity and distribution, do not know what they are losing or have lost. It is impossible to protect something you do not know needs protecting – let alone something you do not even know you have.
Furthermore, it is also difficult to protect something if the reasons why a population is vanishing are unclear. There are many variables to consider when determining the cause of why a lichen is diminishing in population size or range. Identifying the major threat, or threats, to a population or particular lichen “species” as a whole is the first step in addressing the issue. However, having specific microhabitat requirements and being sensitive to minute, and potentially undetectable, changes within the environment, the specific protection requirements for lichens remain largely unknown and extremely difficult to control.
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27
CHAPTER 2. LICHENS OF WHITE PINE HOLLOW STATE PRESERVE
Kathleen M. Thompson and James T. Colbert
Department of Ecology, Evolution, and Organismal Biology
Iowa State University
Ames, Iowa 50011
Abstract
A lichen diversity survey of White Pine Hollow State Preserve in Dubuque County,
Iowa, revealed the presence of 117 different lichens including 13 previously unreported for the State of Iowa, 72 previously unreported for Dubuque County, and three reported in Iowa on only one prior occasion. This increases the number of lichens reported for White Pine
Hollow to 147 and the State of Iowa to a total of 478. Lobaria pulmonaria (L.) Hoffm., an old-growth specialist that is facing declines around the globe, was not amongst the lichens observed although one of the last known collections of this lichen in Iowa occurred at White
Pine Hollow.
Introduction
Despite nearly 150 years of investigation, our understanding of the lichen diversity in
Iowa is far from complete. Extensive landscape alterations were made to the State of Iowa beginning with European settlement in the early 1800s. This included the eventual plowing and conversion of ~99.9% of Iowa’s original 28.6 million acres of prairie to towns and agricultural fields as well as the logging of virtually all of Iowa’s old-growth forest (Smith
1998, Cohen et al. 2001). Unfortunately, we have no knowledge of Iowa’s lichen diversity 28 before 1870. The first recorded lichen for the State of Iowa was Parmotrema crinitum (Ach.)
M. Choisy collected by Charles E. Bessey in 1870 (CNALH 2018). Furthermore, Bohumil
Shimek reported as early as 1915 that the abundance of corticolous lichens in northwest Iowa had decreased (Shimek 1915). These historic collections and observations are of immense importance, as they are part of a very limited set of data we have regarding the lichen diversity of Iowa close to the time of European settlement and during this period of extensive habitat alteration.
Since that time, there have been a handful of efforts to increase our understanding of
Iowa’s lichen diversity and distribution (Bessey 1884, Fink 1895, Fink 1897, Wolden 1935,
Malone and Tiffany 1978, Schutte 1979, Dunlap and Tiffany 1980, Schutte 1983). More recent efforts were carried out by Colbert and Podaril (Colbert 2011, Podaril and Colbert
2015) and resulted in a diversity estimate of 465 lichens for the State of Iowa. A large number of these records, however, are based on only a single accession and were collected prior to the year 1960. Colbert (2011) defined lichens not collected in the state since the year
1960 as likely to be rare in, or potentially extirpated from, the state. Our understanding of
Iowa’s lichen diversity is far from current and comprehensive, highlighting the need for additional investigation.
Area of Study
During the most recent glaciation event approximately 12,000-15,000 years ago, parts of northeast Iowa, as well as southeast Minnesota, southwest Wisconsin, and northwest
Illinois, remained uncovered by glacial ice. This roughly 40,000 km2 landform has been geologically referred to as the “Driftless Area”, or “Paleozoic Plateau”, and is characterized 29 by rugged and rocky topography, steep stream ravines, lack of glacial till, and discontinuous patches of loess soil (Cahayla-Wynne and Glenn-Lewin 1977, Lammers 1983, Hobbs 1999).
As part of the Driftless Area in northwest Dubuque County, White Pine Hollow State
Preserve (288 hectares, established in 1968; Herzberg and Pearson 2001) is uncharacteristic for Iowa in regards to its landscape features and vegetation. In the words of Robert F.
Thorne: “I know of no comparable square-mile area in Iowa that can approach the reserve in the richness of its flora” (Thorne 1964). Exhibiting steep, rocky outcrops and species such as white pine (Pinus strobus L.), canoe birch (Betula papyrifera Marshall), Canada yew (Taxus canadensis Marshall), a rich diversity of bryophytes (Hulbary 1964), as well as the federally- listed northern wild monkshood (Aconitum noveboracense A. Gray ex Coville) and Iowa
Pleistocene snail (Discus macclintocki Baker), White Pine Hollow more closely resembles a boreal habitat than the rich-soiled, rolling hills typical of the vast majority of Iowa (Thorne
1964; Conard 1932a, 1932b). As stated by Henry S. Conard, “[White Pine Hollow] presents a fragment of a vegetation that was once a climax in northeastern Iowa, and doubtless was much richer in species” (Conard 1932b).
White Pine Hollow also boasts the presence of algific talus slopes. An algific talus slope consists of a large, rocky outcrop composed of a permeable layer of dolomite over a layer of semi-permeable limestone, all of which lies over an impermeable layer of shale.
Water is able to seep through the dolomite and form caverns in the limestone. This water slowly freezes throughout the winter months and subsequently slowly melts through the summer months, moderated by internal temperatures. The result is a gradual release of cold air (algific) through crevices between loose rocks (talus) on the outer interface of the outcrop throughout the summer. In addition, warmer water vapor is released throughout the winter. 30
Overall, this effect moderates temperature and moisture levels throughout the year and has been shown to be able to potentially buffer the effects of climate change (Růžička 2015).
Furthermore, it provides habitat for species adapted to more northerly conditions, forming what has been referred to as a “paleorefugium” (Nekola 1999). Considering the rich and rare diversity of plant and animal species, uncharacteristic landscape features, and status as a preserve, it is reasonable to hypothesize that White Pine Hollow State Preserve possesses a high level of lichen diversity that may include rare or unreported lichens for the state.
Before receiving the status of “state preserve” in 1968, a significant portion of the area was logged during the late 1800s to mid 1900s (Fig. 2.1; Johnson 2000). Despite these efforts, White Pine Hollow still maintains a number of oak (Quercus sp.) trees over 200 years old, with one estimated to be as old as 438-458 years (Pearson 1987, Duvick and Blasing
1983). Furthermore, the current stand of white pines (Pinus strobus L.) present at White Pine
Hollow is estimated to be the oldest in northeast Iowa (Pleasants 1994). The majority of trees in this stand date back to the 1860s, and, therefore, likely represent the recovery of a logging, wind, or fire disturbance around this time (Pleasants 1994). Logging on publically-owned property contiguous with White Pine Hollow State Preserve continued into the 1990s (Fig.
2.1).
In addition to its unique geology and ecology, White Pine Hollow is geographically close to locations of important historic lichen collections made in the late 1800s and mid
1900s (CNALH 2018). The first lichen collections at White Pine Hollow were made by
Bohumil Shimek in 1901, though the majority of subsequent collections were made by
Clifford Wetmore in 1965 (49%) and William Weber in 1955 (27%). These important collections serve as a baseline of comparison for future findings at White Pine Hollow and 31 provide the only glimpse we have into the lichen communities of the past. Despite the presence of these historical data, only 74 lichens have been previously reported for White
Pine Hollow from a total of 191 accessions, 82% of which are from 1965 or earlier, and a formal survey of the area has never been conducted. White Pine Hollow is, therefore, no exception to the rest of Iowa with respect to our current understanding of its lichen diversity.
The combination of limited – yet available – archival data and largely outdated collection records not only suggests the need of an updated assessment of White Pine Hollow’s lichen diversity, but it also provides the opportunity to compare current findings to previous records and perhaps observe changes over time.
The two goals of this study were, first, to conduct a lichen diversity survey at White
Pine Hollow, including the possibility of observing the presence of rare or unreported lichens for the State of Iowa. White Pine Hollow is also one of the last known locations for the lichen Lobaria pulmonaria (L.) Hoffm. in Iowa; therefore, the second goal of this study was to expand search efforts for any remaining populations of L. pulmonaria. Lobaria pulmonaria is a sensitive old-growth specialist that suffered major declines throughout the
1900s and is currently decreasing in North America. It is a rather large and impressive lichen that is bright green in color when hydrated and commonly grows on the bark of trees at eye- level, making it a lichen that is easy to notice and collect. Lobaria pulmonaria has been collected in Iowa on four different occasions: once in 1894 and again in 1896 by Bruce Fink, and twice in 1901 by Bohumil Shimek (CNALH 2018). All reported collections were made in northeast Iowa (Fayette, Clayton, and Dubuque County). The most recent of these collections was made by Shimek on May 13th, 1901, in Clayton County. Two days prior, 32
Shimek collected it in White Pine Hollow State Preserve, which is the only L. pulmonaria collection in Iowa with locality information more precise than township.
Lobaria pulmonaria has also been collected in the surrounding states of Minnesota,
Wisconsin, and Illinois (CNALH 2018), which also contain portions of the Driftless Area.
Despite a relatively large number of collections reported to the Consortium of North
American Lichen Herbaria (CNALH) website (www.lichenportal.org) for northern
Minnesota and Wisconsin, L. pulmonaria has only been collected in portions of the Driftless
Area outside of Iowa a total of five times, with all reports located in Wisconsin. The most recent of these collections was made in Monroe County in 1974, with the remaining four made in or prior to the year 1940. The lack of more modern reports of this lichen in the
Driftless Area suggests that L. pulmonaria may be rare in this area – and potentially facing extirpation from the of the Driftless Area in general.
Methods
Lichens were collected at White Pine Hollow on three different occasions: March
15th, 2015, April 9th, 2016, and April 23rd, 2017, totaling 42.5 hours and 79.8 kilometers of search effort. The location of each collection site was determined using a Garmin Dakota 20
GPS device (Fig. 2.2). Spring months were targeted in an attempt to reduce the concealment of lichens by tree foliage and herbaceous vegetation. Habitats surveyed included algific talus slopes, limestone rocks and outcrops, creek beds, deciduous forest, and mixed deciduous- coniferous forest. Though this survey attempted to create a representative list for White Pine
Hollow as a whole, collection emphasis was given to areas hypothesized to contain high levels of lichen diversity as well as rarely or previously unreported lichens for the state – such as the algific talus slopes. In addition, substrates known to contain certain lichens 33 expected to be present in the area based on previous records were sought out, and habitat information was recorded for each of the 105 individual collections made. Special attention was paid to the potentially extirpated lichen, L. pulmonaria, throughout the survey.
Lichens were identified using primarily Brodo (2016), but also Brodo et al. (2001),
Sheard (2010), Smith et al. (2009), Wetmore (2005), as well as various genus-specific keys and species descriptions found on the CNALH. Previously identified lichen accessions present in the Iowa State University Ada Hayden Herbarium (ISC) also aided in the identification of lichens collected at White Pine Hollow. Thin layer chromatography (TLC) was performed on a number of specimens (certain members of the genus Cladonia as well as leprose and sterile crustose lichens) with the assistance of Caleb Morse of the R. L.
McGregor Herbarium at the University of Kansas. Morse also assisted with the identification and verification of other specimens, including Bacidia granosa (Tuck.) Zahlbr., Bacidina delicata (Leighton) V. Wirth & Vězda, Bacidina egenula (Nyl.) Vězda, Caloplaca flavorubescens (Hudson) Søchting, Frödén & Arup, Lecania turicensis (Hepp) Müll. Arg.,
Micarea prasina Fr., Mycoporum pycnocarpoides Müll. Arg., and Thelidium decipiens (Nyl.)
Kremp. Additional lichens that were difficult to identify, such as sterile crusts with no positive chemical tests, were sent to James Lendemer of the New York Botanical Garden.
This included specimens identified by Lendemer to be Bacidia suffusa (Fr.) A. Schneider,
Athallia pyracea (Ach.) Arup, Frödén & Søchting, Varicellaria velata (Turner) Schmitt &
Lumbsch, and Lecanora thysanophora R. C. Harris, as well as a number of specimens that remain indeterminate.
Nomenclature was updated as needed to correspond with Esslinger (2018). Lichens were determined to be new or rare reports for the State of Iowa based on accessions 34 previously reported to the CNALH (2018, accessed: February 19th, 2018). Voucher specimens were deposited in the Ada Hayden Herbarium (ISC) and reported to the CNALH database.
Results
During the three collection trips made to White Pine Hollow State Preserve, 105 individual collections, many with multiple lichens, were made resulting in the identification of 117 different lichens (Table 2.1). Of the lichens identified, 13 were previously unreported for the State of Iowa and three had been reported on only one prior occasion (Table 2.1).
Furthermore, 72 of the 117 identified lichens were previously unreported for Dubuque
County. Two of the identified lichens had not been reported for the State of Iowa since prior to the year 1960: Bacidia granosa (Tuck.) Zahlbr. (1903) and Peltigera ponojensis Gyelnik
(1946). Seventy-one of the 117 lichens identified at White Pine Hollow were represented in the collections made on the algific talus slopes (Table 2.2). Of these, 30 were collected exclusively on algific talus slopes, including 4 of the 13 newly reported lichens (~30%). The addition of 13 newly reported lichens increases our previous estimate of the lichen diversity in Iowa from 465 lichens (Podaril and Colbert 2015) to 478.
Prior to this study, 191 lichen accessions had been reported for White Pine Hollow to the Consortium of North American Lichen Herbaria (CNALH 2018) with 82% having been collected in 1965 or earlier. Once the listed accession names were compared to current nomenclature (Esslinger 2018), the number of lichens previously reported for White Pine
Hollow dropped from 84 to 74. Forty-four of these 74 lichens were also observed during this study, leaving 30 of the previously reported lichens not found by the present survey. The list 35 of previously reported lichens was combined with those identified in this study for a list totaling 147 lichens reported for White Pine Hollow State Preserve (Table 2.1).
As the last known specific location of occurrence of in Iowa, as well as the presence of adequate substrate (deciduous trees such as A. saccharum) and status as a preserve, it is reasonable to hypothesize that if populations L. pulmonaria are persisting in Iowa, they might be doing so at White Pine Hollow. In 2011, Colbert logged 67.8 kilometers within 11 locations throughout northeast Iowa, including White Pine Hollow, in search of L. pulmonaria but had no success (Colbert 2011). Though special effort, including 79.8 additional kilometers of search effort, was made to search for L. pulmonaria throughout the survey, this lichen was not found at White Pine Hollow.
Discussion
The purpose of this study was to develop a more complete and current inventory of the lichen diversity at White Pine Hollow State Preserve, including potentially rare or previously unreported lichens for Dubuque County and the State of Iowa. Integration of the
117 lichens observed in this study with previous data brings the total number of lichens reported for White Pine Hollow to 147. This corresponds to ~31% (147/478) of the lichen diversity that has been reported for the entire State of Iowa present in an area of only 288 hectares.
Thirteen of the lichens identified in this study were previously unreported for Iowa, increasing the total number of distinct lichens reported for the state to 478 from the previous estimate of 465 lichens (Podaril and Colbert 2015). Prior to 2015, our estimate of the lichen diversity in Iowa was 448 lichens (Colbert 2011). Therefore, within less than 10 years time,
30 previously unreported lichens have been identified for the state. It is possible that this list 36 is nearing an accurate inventory of the lichen diversity in Iowa given the lichen diversity estimates of surrounding states (Nebraska: 411 lichens, Egan et al. 2002; Wisconsin: 726 lichens, Bennett 2006; Minnesota: 780 lichens, Bennett and Wetmore 2004; southeast
Missouri: 181 lichens, Peck et al. 2004).
There are, however, quite likely to be other lichens that remain undiscovered and have yet to be reported for Iowa. Furthermore, as our understanding of lichen taxonomy and species delimitations increases, it is probable that this estimate will increase due to cryptic lichens currently being listed under more inclusive names (Lücking et al. 2016). Conversely, it is possible that some of the lichens included in this list, particularly those reported on only one previous occasion, were incorrectly identified – leading to a reduction in this estimate. It is also possible that some of the lichens included in the current estimate have since been extirpated from the state and are no longer a part of the current diversity of lichens in Iowa.
Podaril and Colbert (2015) estimated that 33 macrolichens, or those that are relatively large and, therefore, more conspicuous, reported for Iowa were either rare or potentially extirpated.
Of the 13 newly-reported lichens for Iowa, eight are crustose (Arthonia diffusa Nyl.,
Arthonia lapidicola [Taylor] Branth & Rostrup, Bacidina delicata [Leighton] V. Wirth &
Vězda, Lecania turicensis [Hepp] Müll. Arg., Mycoporum pycnocarpoides Müll. Arg.,
Rinodina ascociscana [Tuck.] Tuck., Rinodina subminuta H. Magn., and Thelidium decipiens
[Nyl.] Kremp.), two are leprose (Botryolepraria lesdainii [Hue] Canals, Hernández-Mariné,
Gómez-Bolea & Llimona and Leproplaca chrysodeta [Vainio] J. R. Laundon ex Ahti), one is squamulose (Agonimia tristicula [Nyl.] Zahlbr.), and two are foliose (Peltigera membranacea [Ach.] Nyl. and Physconia muscigena [Ach.] Poelt). The finding of unreported foliose lichens is particularly interesting due to their size and, therefore, noticeability – 37 especially that of the relatively large P. membranacea. However, the observation of B. lesdainii is also significant due to its high abundance at White Pine Hollow. It was present in relatively large quantities and in multiple collections. This seemingly-leprose lichen is visually distinguishable from Lepraria finkii (B. de Lesd.) R. C. Harris by its deeper green color and lack of true soredia; it can be also be determined chemically by the presence of the triterpenoid lesdainin detected via TLC (Canals et al. 1997). It is possible that this lichen has been previously unreported due to lack of recent collection effort in that portion of the state – particularly since the lichen’s original description did not occur until 1987 under the name
Lepraria lesdainii (Hue) R.C. Harris. It is also possible that given the effort involved in TLC, it has been previously misidentified as L. finkii or Lepraria membranacea (Dickson) Vainio based on morphological characters.
According to the CNALH, there are only 37 herbarium accessions of the lichen A. tristicula collected in the US – with a number of these appearing to be part of mutual collection occurrences. The majority of these collections were made in Colorado and the
Pacific Northwest; however, this report of A. tristicula constitutes the seventh collection in the Midwest. Surprisingly, this lichen was collected multiple times throughout this study – and often by accident. Agonimia tristicula is a small, squamulose lichen that grows on soil and mosses, has black, barrel-shaped perithecia, and beautiful, brown muriform spores.
Given its small size, it is possible that this lichen is much more common and widespread than reports indicate.
In addition to the first-reports of 13 lichens for the State of Iowa, this study also made second-reports for three lichens: P. ponojensis, Pertusaria consocians Dibben, and Strigula stigmatella (Ach.) R. C. Harris. Furthermore, two of the identified lichens, including one of 38 the second-reports (P. ponojensis), had not been reported for Iowa since prior to the year
1960: B. granosa (1903) and P. ponojensis (1946). These lichens were, therefore, considered to be potentially rare or extirpated from the State of Iowa (Colbert 2011). Collection of these two lichens suggests that, while they may be rare in the state, they are not extirpated.
Peltigera ponojensis has a distribution that includes more northern latitudes and higher elevations than that of Iowa. It is possible that P. ponojensis is able to persist in the northeast-corner of the state due to the presence of the aforementioned algific talus slopes, which create a habitat that more closely resembles that of boreal latitudes or higher elevations. Bacidia granosa is part of a group of distinct lichens that, until recently, were all referred to as Bacidia coprodes (Körber) Lettau (Ekman 2014). However, B. granosa is distinct from B. coprodes due to the presence of a hypothecium that is paler than the surrounding exciple. Bacidia coprodes has been reported for the State of Iowa 50 times prior to this study, with the most recent collection made in 2013 (CNALH 2018). Given the relatively recent reclassification within this group, it is possible that many of these B. coprodes accessions are, in fact, B. granosa.
As previously mentioned, collection emphasis was given to areas thought to harbor high levels of lichen diversity as well as rare or previously unreported lichens for the State of
Iowa; this included, particularly, the algific talus slopes. Seventy-one of the 117 total reported lichens (~61%) were represented in the collections made on the algific talus slopes.
Though this high concentration of distinct lichens may be a result of a high level of diversity present, it may also be partially attributed to collection bias. However, 30 of the 71 lichens represented were collected only on the algific talus slopes (Table 2.2), with 4 of the 13 newly 39 reported lichens for Iowa being among these (A. lapidicola, M. pycnocarpoides, P. membranacea, P. muscigena).
According to collections reported by the CNALH, the nearest populations of P. muscigena and P. membranacea to the State of Iowa are in northern Wisconsin and central to northern Minnesota (CNALH 2018). It is possible that these two lichens are only able to persist in Iowa due to the unique microhabitat created by the algific talus slopes. All eight of the collections of Scytinium lichenoides (L.) Otálora, P. M. Jørg. & Wedin were made on the algific talus slopes, suggesting that they may play an important role in the presence of this lichen at White Pine Hollow. Scytinium lichenoides is described as growing primarily in montane forests (Nash et al. 2004); however, there also appear to be a significant number of collections in the Ozarks and northern Midwest (CNALH 2018). Also included in this list is
P. ponojensis, which was collected only once in this survey. This further suggests that P. ponojensis may only be able to persist in the State of Iowa due to the presence of algific talus slopes, as proposed above.
In addition to the 117 lichens identified, eight specimens remain unable to be identified using morphological and chemical techniques. Included in these eight specimens are two perithecial lichens, three pycnidial lichens, and three sterile lichens – all of which are crustose. Both of the perithecial lichens appear to be devoid of spores, though two of the pycnidial lichens contain conidia, and two of the sterile lichens are producing soredia.
Interestingly – through not necessarily surprisingly – five of the eight indeterminate specimens were collected on the algific talus slopes. This suggests that this particular type of microhabitat is likely understudied and may harbor lichens that are rare and potentially not yet described. 40
Of the 30 lichens previously reported for White Pine Hollow that were not found in this study, five are unique to White Pine Hollow in regards to their collection in Iowa
(Arthonia sanguinea Willey, Biatora vernalis [L.] Fr., Phaeophyscia erythrocardia [Tuck.]
Essl., Lepra ophthalmiza [Nyl.] Hafellner, and Graphis caesiella Vainio), with four of the five having only been collected once (Table 2.1). It is possible that these lichens have or had a limited distribution in Iowa and were either missed during this most recent search effort or have since been extirpated from the area. However, its also possible these specimens have been misidentified. For example, the lichen A. sanguinea is only known to occur at locations subjected to coastal fogs and is often mistaken with Arthothelium spectabile (Flotow) A.
Massal. (Nash et al. 2007) – a lichen that has been commonly collected in Iowa, including this most recent study at White Pine Hollow. It is possible that this specimen was misidentified and could be more accurately placed under the name A. spectabile. However, the specimen itself, located at the Santa Barbara Botanic Garden Lichen Herbarium (SGGB), would need to be revisited to verify.
This study also aimed to either locate extant populations of L. pulmonaria persisting at White Pine Hollow or to provide further evidence supporting its extirpation from the state.
At the conclusion of this study, L. pulmonaria remains unreported for the State of Iowa since
1901. Given that this lichen is large and often visible at eye-level, it is likely that if it were persisting at White Pine Hollow, it would have been located. The lack of discovery adds further evidence that L. pulmonaria has been extirpated from White Pine Hollow and the
State of Iowa. Unfortunately, given the limited available data, we cannot make any confident inferences as to why L. pulmonaria is no longer part of Iowa’s current diversity. Its lack of discovery, however, poses this question: what else are we losing – or have we lost? Had Fink 41 and Shimek not made these collections roughly 120 years ago, we would never have known that L. pulmonaria existed in the State of Iowa and comprised a component of Iowa’s assemblage of native biodiversity.
The addition of 13 newly reported lichens for Iowa and the rediscovery of two rare or potentially extirpated lichens indicates that there is still much we have yet to learn about the lichen diversity and distribution in Iowa. With the current amount of environmental change taking place, it is becoming increasingly important to know “what” is “where” and be able to track these changes over time. In addition, it is important to identify which lichens are rare or in danger of extirpation from the state. Though lichens may not abide by geopolitical boundaries, decisions regarding land-use management and species conservation are often made at the state level. The usefulness of the overall information gathered in this study will go well beyond that of the aforementioned goals and may also be of potential value in developing a management plan for White Pine Hollow State Preserve that includes its lichen diversity.
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Tables
Table 2.1 Lichens of White Pine Hollow State Preserve (WPH) reported previously to the CNALH (accessed February 19th, 2018) or observed during this study. Names were updated to Esslinger 2018 (accessed February 12th, 2018). *Deprecated name, but varieties not specified.
Current Previously # Previous Most Recent New for New for Scientific Name WPH Reported for IA Previous IA Dubuque Co. Iowa Findings WPH Accessions Collection Acrocordia cavata X X 16 2015 Agonimia tristicula X X X 0 Alyxoria varia X X 158 2017 Amandinea dakotensis X X 49 2013 Anaptychia palmulata X 15 1979 Anisomeridium polypori X X 19 2013 Arthonia diffusa X X X 0 45
Arthonia lapidicola X X X 0 Arthonia patellulata X X 13 2013 Arthonia punctiformis X 64 2005 Arthonia radiata X 100 2013 Arthonia sanguinea X 1 1965 Arthothelium ruanum X X 7 2011 Arthothelium spectabile X X 59 2013 Athallia holocarpa X X 70 2015 Athallia pyracea X X 18 2015 Bacidia circumspecta X X 13 2017 Bacidia granosa X X 2 1903 Bacidia polychroa X X 54 1994
Table 2.1 Continued.
Current Previously # Previous Most Recent New for New for Scientific Name WPH Reported for IA Previous IA Dubuque Co. Iowa Findings WPH Accessions Collection Bacidia rubella X X 32 2017 Bacidia suffusa X X 65 2013 Bacidina delicata X X X 0 Bacidina egenula X X 15 2014 Bagliettoa calciseda X X 6 2010 Biatora vernalis X 1 1955 Bilimbia sabuletorum X X 65 2013 Botryolepraria lesdainii X X X 0 Calogaya lobulata X 6 2017 Caloplaca atroalba X X 5 2008
46
Caloplaca cerina X X 202 2016 Candelaria concolor X X 246 2016 Candelaria fibrosa X X 90 2017 Candelariella efflorescens X X 9 2013 Catillaria nigroclavata X X 7 2013 Chrysothrix caesia X X 157 2017 Cladonia coniocraea X X 33 2014 Cladonia cylindrica X X 3 1961 Cladonia didyma X X 17 2007
Table 2.1 Continued.
Previously Most Recent Current WPH New for # Previous IA Scientific Name Reported for New for Iowa Previous IA Findings Dubuque Co. Accessions WPH Collection Cladonia macilenta X X 42 2017 Cladonia macilenta var. bacillaris X 9 2007 Cladonia parasitica X 74 2013 Cladonia ramulosa X X 6 1983 Cladonia squamosa X 39 2012 Dermatocarpon luridum X 6 2014 Dermatocarpon miniatum X X 145 2014 Dermatocarpon muhlenbergii X X 3 1965 Endocarpon pallidulum X X 16 2015 Eopyrenula intermedia X X 24 2015 Flavoparmelia baltimorensis X 10 2013 47
Flavoparmelia caperata X X 156 2016 Flavoplaca citrina X X 40 2016 Flavoplaca flavocitrina X 4 1991 Flavopunctelia flaventior X 10 2006 Flavopunctelia soredica X 3 1978 Graphis caesiella X 2 1955 Graphis scripta X X 269 2017 Gyalolechia flavorubescens X X 139 2017
Table 2.1 Continued.
Previously Most Recent Current WPH New for # Previous IA Scientific Name Reported for New for Iowa Previous IA Findings Dubuque Co. Accessions WPH Collection Gyalolechia flavovirescens X X 83 2013 Heterodermia speciosa X 50 2011 Hyperphyscia adglutinata X 72 2011 Hyperphyscia syncolla X X X 168 2017 Lecania turicensis X X X 0 Lecanora appalachensis X X 6 2017 Lecanora chlarotera X 11 2013 Lecanora strobilina X X 22 2017 Lecanora thysanophora X X 16 2014 Lecidella stigmatea X X 3 1967 Lepra ophthalmiza X 1 1965 48
Lepraria finkii X X 97 2017 Lepraria membranacea X 37 1986 Leproplaca chrysodeta X X X 0 Leptogium cyanescens X X X 23 2011 Lobaria pulmonaria X 13 1901 Melanelixia subaurifera X 11 1978 Micarea prasina X X 3 2007 Mycoporum pycnocarpoides X X X 0
Table 2.1 Continued.
Previously Most Recent Current WPH New for # Previous IA Scientific Name Reported for New for Iowa Previous IA Findings Dubuque Co. Accessions WPH Collection Myelochroa aurulenta X X 87 2017 Myelochroa galbina X X 49 2013 Myriolecis sambuci X X 2 2015 Parmelia saxatilis X 17 1980 Parmelia sulcata X X 30 2004 Parmotrema hypotropum X X 12 2013 Parmotrema margaritatum X 39 2011 Parmotrema perforatum X 16 1978 Parmotrema perlatum X 11 2013 Parmotrema reticulatum X X 30 2014 Peltigera canina X X 113 1996 49
Peltigera elisabethae X 10 1965 Peltigera evansiana X X 37 2011 Peltigera membranacea X X X 0 Peltigera polydactyla* X 19 1966 Peltigera ponojensis X X 1 1946 Peltigera praetextata X X 42 2014 Peltigera rufescens X X 63 2013 Pertusaria consocians X X 1 1993
Table 2.1 Continued.
Previously Most Recent Current WPH New for # Previous IA Scientific Name Reported for New for Iowa Previous IA Findings Dubuque Co. Accessions WPH Collection Pertusaria macounii X X 3 2016 Pertusaria pustulata X X 68 2013 Phaeophyscia adiastola X X 68 2017 Phaeophyscia ciliata X X 193 2017 Phaeophyscia erythrocardia X 1 1980 Phaeophyscia hirsuta X X X 77 2017 Phaeophyscia hirtella X X 29 2012 Phaeophyscia hispidula X X 18 1996 Phaeophyscia orbicularis X X 58 2015 Phaeophyscia pusilloides X X 39 2017 Phaeophyscia rubropulchra X X 76 2013 50
Physcia aipolia X X 161 2017 Physcia americana X X 65 2017 Physcia millegrana X X 150 2015 Physcia stellaris X X 335 2017 Physciella chloantha X 100 2017 Physciella melanchra X X 29 2015 Physconia detersa X X 56 2016 Physconia leucoleiptes X 102 2017
Table 2.1 Continued.
Previously Most Recent Current WPH New for # Previous IA Scientific Name Reported for New for Iowa Previous IA Findings Dubuque Co. Accessions WPH Collection Physconia muscigena X X X 0 Placopyrenium fuscellum X X 45 1996 Placynthium nigrum X X 46 2007 Polycauliona candelaria X 36 1994 Protoblastenia rupestris X X 12 2008 Punctelia bolliana X X 197 2015 Punctelia rudecta X X 239 2017 Pyrenula pseudobufonia X X 35 2017 Pyxine sorediata X X 32 2013 Ramalina americana X X 72 2016 Rinodina ascociscana X X X 0 51
Rinodina populicola X X 36 2015 Rinodina subminuta X X X 0 Sarcogyne regularis X X 21 2015 Scoliciosporum chlorococcum X X 10 2012 Scytinium dactylinum X X 43 1991 Scytinium lichenoides X X 69 2014 Squamulea subsoluta X X 83 2016 Strigula stigmatella X X 1 2014
Table 2.1 Continued.
Previously Most Recent Current WPH New for # Previous IA Scientific Name Reported for New for Iowa Previous IA Findings Dubuque Co. Accessions WPH Collection Teloschistes chrysophthalmus X X 146 2017 Thelidium decipiens X X X 0 Tuckermannopsis ciliaris X 23 1955 Varicellaria velata X X 78 1967 Verrucaria calkinsiana X X 12 2015 Verrucaria glaucovirens X X 4 1996 Verrucaria muralis X X 48 2013 Verrucaria nigrescens X X 42 2013 Willeya diffractella X X 21 2013 Xanthocarpia feracissima X 57 2015 Xanthomendoza fallax X X 139 2016 52
Xanthomendoza hasseana X X 62 2015 Xanthomendoza ulophyllodes X X 67 2017 Xanthomendoza weberi X X 95 2017
Totals: 3 of the lichens observed in this study have 147 117 74 72 13 been reported only once previously in Iowa
53
Table 2.2 Complete list of lichens collected on algific talus slopes, as well as the percentage of collections of each distinct lichen made on the algific talus slopes. Species in bold print are newly reported for the State of Iowa.
% of Collections on Collected Only on Scientific Name Algific Talus Slopes Algific Talus Slopes (Total # of Collections) Agonimia tristicula 75% (4) Amandinea dakotensis X 100% (2) Arthonia lapidicola X 100% (1) Arthothelium spectabile 33% (3) Bacidia coprodes 67% (3) Bacidia granosa 50% (4) Bacidia rubella X 100% (2) Bagliettoa calciseda 50% (2) Bilimbia sabuletorum 80% (5) Caloplaca atroalba X 100% (2) Caloplaca cerina 25% (8) Caloplaca chrysodeta X 100% (1) Caloplaca feracissima X 100% (1) Caloplaca holocarpa X 100% (1) Caloplaca subsoluta X 100% (5) Candelaria concolor 20% (10) Candelaria fibrosa X 100% (2) Candelariella efflorescens 25% (4) Catillaria nigroclavata 29% (7) Chrysothrix caesia 33% (3) Cladonia ramulosa 33% (3) Dermatocarpon miniatum 33% (3) Dermatocarpon muhlenbergii 50% (2) Endocarpon pallidulum 67% (3) Flavoplaca flavocitrina X 100% (1) Flavopunctelia flaventior X 100% (1) Graphis scripta 20% (10) Gyalolechia flavorubescens 33% (3) Gyalolechia flavovirescens X 100% (5) Hyperphyscia syncolla 20% (5) Lecanora appalachensis X 100% (2) Lecanora thysanophora 67% (3) Lecidella stigmatea X 100% (1) Lepraria finkii 43% (7) Leptogium cyanescens 25% (4) 54
Table 2.2 Continued.
% of Collections on Collected Only on Scientific Name Algific Talus Slopes Algific Talus Slopes (Total # of Collections) Mycoporum pycnocarpoides X 100% (1) Myelochroa galbina X 100% (1) Peltigera canina X 100% (3) Peltigera membranacea X 100% (1) Peltigera ponojensis X 100% (1) Peltigera praetextata X 100% (1) Peltigera rufescens X 100% (1) Pertusaria consocians 14% (7) Phaeophyscia adiastola 50% (12) Phaeophyscia ciliata 20% (5) Phaeophyscia hispidula 33% (3) Phaeophyscia pusillioides 50% (2) Phaeophyscia rubropulchra 20% (5) Physcia aipolia 25% (4) Physcia stellaris 14% (7) Physconia detersa 13% (8) Physconia muscigena X 100% (1) Placopyrenium fuscellum 60% (5) Placynthium nigrum X 100% (1) Protoblastenia rupestris 80% (5) Punctelia rudecta 14% (7) Pyrenula pseudobufonia X 100% (1) Ramalina americana 43% (8) Rinodina subminuta 13% (8) Sarcogyne regularis X 100% (1) Scoliciosporum chlorococcum X 100% (1) Scytinium lichenoides X 100% (8) Squamelea subsoluta 80% (5) Strigula stigmatella X 100% (1) Verrucaria calkinsiana 60% (5) Verrucaria glaucovirens X 100% (3) Verrucaria muralis 63% (8) Verrucaria nigrescens 85% (13) Xanthomendoza fallax X 100% (1) Xanthomendoza hasseana 33% (6) Xanthomendoza ulophyllodes 17% (6)
55
Figures
Figure 2.1 Map illustrating past disturbances in White Pine Hollow State Preserve in Dubuque County, Iowa, including the prevalence of logging. Adapted from the White Pine Hollow State Preserve Ecological Management Plan (Johnson 2000).
56
Figure 2.2 Map showing location of collections made at White Pine Hollow State Preserve, Dubuque County, Iowa. The size of the point correlates with the number of collections made at each particular location. 57
CHAPTER 3. ASSESSING THE REINTRODUCTION POTENTIAL OF THE NATIVE IOWA LICHEN LOBARIA PULMONARIA
Kathleen M. Thompson and James T. Colbert
Department of Ecology, Evolution, and Organismal Biology
Iowa State University
Ames, Iowa 50011
Abstract
The lichen Lobaria pulmonaria (L.) Hoffm. suffered tremendous population declines throughout Europe in the 1900s and is currently decreasing in North America. An example of this decrease is the loss of its range extending into the State of Iowa. One of the most recent collections of this lichen in Iowa was made at White Pine Hollow State Preserve in 1901.
This study attempted to gauge the potential for success of a reintroduction of L. pulmonaria to its historic range in northeast Iowa. Asexual propagules, including soredia and isidia, and young thalline lobes were applied to Acer saccharum Marshall bark from White Pine Hollow and monitored for 12 months under greenhouse conditions. At the conclusion of the study, no growth had occurred in any of the treatments. The difficulty in propagating L. pulmonaria under controlled conditions emphasizes the need for greater protection efforts of this lichen, as well as others, in locations where they remain present.
Introduction
One of the more well-known lichens with regard to conservation status is Lobaria pulmonaria. Lobaria pulmonaria is a large, foliose lichen that is bright green when hydrated.
It tends to grow at eye-level and is, therefore, rather conspicuous – particularly with respect 58 to other lichens. Though previously common throughout northern temperate and boreal regions, populations of L. pulmonaria experienced a notable decline during the 1900s and are now considered to be endangered in Central Europe as well as other industrialized countries
(Scheidegger et al. 1998). As early as 1969, L. pulmonaria was considered to be extinct from the Netherlands (Barkman 1969), and is now reported to be declining in most of northern
Europe (Öckinger et al. 2005).
Possessing one of the highest sensitivity levels to sulfur dioxide (SO2; Türk et al.
1974; Nash 1976), it is thought that the disappearance of L. pulmonaria in developed and industrialized areas is the result of increased concentrations of SO2 due to the burning of fossil fuels (Richardson 1992). Additionally, this lichen is known to be sensitive to acid rain
(Sigal and Johnston Jr. 1986) and ozone (Scheidegger & Schroeter 1995). It has also been noted that even in “clean-air” conditions, the range of this lichen is continuing to diminish
(Scheidegger et al. 1998), indicating that air pollution is not the only factor participating in its demise.
Another major threat to this lichen is habitat disturbance and fragmentation. Lobaria pulmonaria is an old-growth specialist and has historically been used as an indicator of habitat quality and continuity (Campbell and Fredeen 2004, Nascimbene et al. 2010, Rose
1976, Gauslaa 1994, Kuusinen 1996). Its specificity for old-growth forests is thought to be due primarily to poor dispersal ability (Sillett et al. 2000, Wasler 2004, Öckinger et al. 2005); however, factors related to habitat quality, such as tree circumference and amount of bryophyte coverage, have also been shown to be important (Öckinger et al. 2005). Lobaria pulmonaria is also sensitive to high levels of UV radiation – particularly when dry (Gauslaa and Solhaug 1999). This creates a critical balance between light availability for growth and 59 risk of desiccation and UV damage (Gauslaa et al. 2006), which likely also plays a role in the confinement of this lichen to stable, old-growth habitats.
Unfortunately, the amount of undisturbed forest is continuing to decline across the globe due to anthropogenic causes (Parviainen 2005, Foster et al. 1997, Sodhi 2009).
Temperate forests throughout Europe and North America were historically cleared for human settlement and continue to be logged today for timber, paper, and other products. Lobaria pulmonaria, like any species, is susceptible to the loss of habitat. However, this lichen is also particularly vulnerable to habitat disturbances, which often include forest management procedures. Lobaria pulmonaria has been shown to be extremely sensitive, with regard to both abundance and fertility, to traditional clear-cutting forestry techniques and even green- tree retention practices, where live trees are left standing specifically in an attempt to maintain biodiversity (Edman et al. 2008). One study, however, found better vitality of L. pulmonaria when clusters of trees were left standing as opposed to scattered individuals
(Hazell and Gustafsson 1999). This result could be due to the aforementioned dispersal limitations, changes in microhabitat qualities, or a combination of these two factors.
A number of conservation efforts have been employed in an attempt to protect and manage L. pulmonaria, including propagation and translocation experiments. The
International Union for Conservation of Nature (IUCN) describes conservation translocation to be “the deliberate movement of organisms from one site for release in another” (IUCN
2013). The term “translocation” will continue to be used in a similarly general sense throughout this section, as it appears that this term along with “relocation” and
“transplantation” are used rather interchangeably in the lichen conservation literature. 60
Lichen translocation programs have been performed since the 1950s (Hale 1950,
1954), though more specifically for the purpose of conservation biology starting in the 1960s
(Brodo 1961, Rao and LeBlanc 1966, LeBlanc and Rao 1973). The methods utilized in these studies included cutting discs of bark containing lichen thalli from trees and transferring them to trees in other locations to assess the effects of SO2 from industrialized areas on lichens. The first translocation experiment involving L. pulmonaria appears to have been conducted by Hawksworth in 1971 (Hawksworth 1971). The purpose of this study was to see whether L. pulmonaria was able to persist in an area where it was thought to be common prior to the year 1900. Unfortunately, the translocated thalli began to slowly discolor and eventually fell from the transplanted bark plugs after about 19 months. Gilbert reported in
1977 that only 30% of 25 translocated L. pulmonaria individuals survived after a three-year period, with most of them falling off of the bark or being killed by the adhesive used for attachment (Gilbert 1977). Denison reported success with growing translocated L. pulmonaria thalli on nylon monofilament in 1988 (Denison 1988). In 1990, Hallingbäck propagated L. pulmonaria to Acer platanoides L. using soredia, isidia, and thallus fragments with the specific “aim to rescue an endangered lichen” (Hallingbäck 1990). After a year, there were hundreds of small thalli roughly 5x5mm in size, which grew to 12x10mm by 18 months. Apparently by the year 2008, thalli could also be found on neighboring trees (Smith
2014). Scheidegger reported on the development of translocated asexual propagules of L. pulmonaria in 1995 (Scheidegger 1995), and he and others published the results of a successful translocation experiment that same year involving L. pulmonaria as well as two additional threatened lichens: Sticta sylvatica (Hudson) Ach. and Parmotrema crinitum
(Ach.) M. Choisy (Scheidegger et al. 1995). There have been a number of translocation 61 efforts for other Lobaria species as well (Gilbert 1991, Sillett and McCune 1998,
Hallingbäck and Ingelög 1989 [as described in Smith 2014]).
Though L. pulmonaria is still relatively common and widespread in North America
(and is, therefore, not currently listed as threatened or endangered), it is currently declining
(Brodo et al. 2001). One example includes its likely extirpation from the State of Iowa since its last collection in 1901 (Colbert 2011; see Chapter 2). It is possible that the difference in status between North America and Europe is due to Europe’s more extensive history with forest management and the effects of industrialization (Edman et al. 2008). Had L. pulmonaria not been so large and conspicuous, it is likely that its decline throughout Europe, as well as North America and Iowa, would have proceeded with little to no notice – perhaps as many other unnoticed lichens have, unfortunately, done. Lobaria pulmonaria has, in some ways, served as a gateway to the recognition of lichens as organisms in need of conservation attention: it is accessible due to its size and ease of identification, it has discernible ecological roles, and it lends itself to conservation experimentation by way of its relatively rapid rate of growth and presence of asexual propagules (soredia and isidia). Unfortunately, most other lichens do not fit this description. Nevertheless, as indicators of habitat quality and continuity in a continually degrading and ever-changing world, monitoring populations of L. pulmonaria and learning how to best manage this lichen will become increasingly important.
Lobaria pulmonaria was last collected in Iowa on May 13th, 1901 in Clayton County; two days prior, it was collected at White Pine Hollow State Preserve in neighboring Dubuque
County. This collection is the only one of the four total collections of L. pulmonaria made in
Iowa that has locality information more specific than township. Though the exact cause of its extirpation from Iowa is unknown, there are some likely suspects. As mentioned, L. 62 pulmonaria has been used as an indicator of habitat quality and continuity. Much like its prairies, Iowa’s forested land was quickly converted to agricultural fields after European settlement in the early 1800s. By the year 1875, only 2.1 million of the original 7 million acres of woodland remained (Cohen et al. 2001). Furthermore, it has been reported that many lichens associated with old-growth forests are limited by their dispersal abilities, including L. pulmonaria (Sillett et al. 2000, Wasler 2004, Öckinger et al. 2005). Given these factors, it is possible that the clear cutting of Iowa’s forests, including the logging of a significant portion of White Pine Hollow (Johnson 2000; Fig. 2.1), not only reduced and fragmented the available habitat for subsequent generations of L. pulmonaria, but it may have also diminished population sizes and propagule loads to critically low levels.
Another factor to consider is the increased use in agricultural chemicals as well as general declines in air quality throughout Iowa in the last century. Currently, Iowa’s sulfur and nitrogen deposition levels are amongst the highest in the country (NADP 2015). In addition to its role as an indicator of habitat quality and continuity, L. pulmonaria has been used as an indicator of air quality due to its low tolerance for certain chemicals, such as those containing sulfur and high levels of nitrogen as well as the certain classes of herbicides
(Jansen et al. 1999, Jovan 2008). Furthermore, Colbert (2011) noted that roughly 36% of the potentially rare or extirpated lichens reported for Iowa at that time were cyanolichens, which includes L. pulmonaria. Given that they constitute only 10% of all lichens globally, this observation may suggest that cyanolichens are particularly vulnerable to the changes that have taken place in Iowa throughout the last decade (Colbert 2011). It is also possible that changes as a result of global climate change have played a role in the likely extirpation of this lichen. 63
Unfortunately, given the limited available data, we cannot make any confident inferences as to why L. pulmonaria is no longer part of Iowa’s current assemblage of biodiversity. This study aimed to provide insight as to whether L. pulmonaria’s extirpation was the result of reduced population size and propagule load due to habitat loss and overharvesting or if it was the result of some sort of environmental change, such as a decrease in air quality. In other words: if young individuals as well as asexual propagules, including soredia and isidia, of L. pulmonaria were translocated to White Pine Hollow, could a population be established and persist? Would a reintroduction of L. pulmonaria to its historic range in northeast Iowa be successful given the current conditions at White Pine
Hollow? To approach these questions, the establishment success of asexual propagules and young thalline lobes of L. pulmonaria on sugar maple bark (Acer saccharum Marshall) from
White Pine Hollow was assessed.
Methods
Collections of L. pulmonaria were made on July 30th, 2016 from a robust population located near Sucker Bay in Chippewa National Forest, Minnesota. Seven total collections were made, totaling ~160 grams of propagation material. Information such as substrate, habitat, temperature, humidity, wind speed, and light intensity were recorded for each collection and measured using a Brunton Sherpa device and the iPhone application
LightMeter. Location and elevation information was recorded using a Garmin Dakota 20
GPS device. Five of the seven collections were made from the bark of white cedar (Thuja occidentalis L.), while the remaining two were collected from ash (Fraxinus sp.) and white spruce (Picea glauca [Moench] Voss). White cedar bark devoid of L. pulmonaria thalli was collected from Chippewa National Forest to serve as a control substrate, and sugar maple 64
(Acer saccharum) bark was collected from White Pine Hollow for experimental propagation treatments. The sugar maple bark was rather recalcitrant and required the use of a draw knife for removal. Bark from Chippewa National Forest and White Pine Hollow were attached to
10x10cm wooden squares using Gorilla Glue as well as stainless steel staples as needed.
Lichen collections were stored at room temperature for ~6.5 weeks before propagules were collected.
Asexual propagules, including both soredia and isidia, were collected in unison with a
#8 “shader” style paintbrush in which the bristles had been trimmed to maximize dexterity and minimize propagule loss. The mix of propagules was sieved through an 850μm sieve to be sure no thallus fragments or small lobes were included. Propagules were added to a total of eight randomly assigned bark samples – four from Chippewa National Forest and four from White Pine Hollow – by gently rubbing them into the crevices of the dampened bark. A gauze-treatment similar to Scheidegger et al. (1995) was attempted, though propagules did not seem to sit well between the gauze fibers: propagules were either pushed behind the gauze, and therefore not visible for observation, or washed off the front of the gauze with the initial watering. It is possible this gauze was a slightly different weave than that used by
Scheidegger et al.
Young, or small, thalline lobes were collected using fine-point forceps and added to four randomly chosen bark samples from each location by manually securing them into bark crevices. Care was given to equally distribute the number and sizes of young lobes between the eight bark samples. Adult thalli were attached using stainless steel staples to four randomly chosen bark samples from each location. Each sample received both a portion of uninjured adult thallus (one that had not had propagules and lobes removed) as well as 65 injured adult thallus. These were included to serve as a control and provide insight as to whether previously established L. pulmonaria individuals would be able to survive the provided greenhouse conditions. Eight additional bark samples, four with bark from each of the two locations, received no treatment and served as general controls to verify that any observed growth of L. pulmonaria was the result of a propagation treatment as opposed to propagules present beforehand. The 64 total bark samples were attached to eight wooden boards with each containing one representative of the eight total treatments (Fig. 3.1). This was done using Velcro so each bark sample could be easily removed for observation, measurement, and photographing. The location of each treatment on each board was randomized to avoid any spatial bias due to environmental factors in the greenhouse.
The boards were stored in moderate conditions with regard to light and temperature and were misted with distilled water at least once each day for one week before being moved to their permanent location in the greenhouse. A wooden frame was constructed which suspended the boards in two rows with metal hooks (Fig. 3.2), allowing them to also be removed for transport or observation if needed. Plastic troughs were initially added below the upper row of boards in an attempt to ensure no propagules were traveling from one board to another. A site in the greenhouse to hang the frame was assessed for suitable habitat qualities such as light intensity, humidity, and temperature. Light intensity was measured using the iPhone LightMeter application for an instantaneous measurement and HOBO Light Intensity
Data Loggers for a 48-hour period to get a better idea of the maximum light intensity reached over a 24-hour period. The maximum light intensity reading in the field was 1,153 lux, whereas the maximum greenhouse reading was 46,845 lux. It is possible that the large difference in readings was due to measuring at different times of the day or comparing 66 measurements from two different devices (as the LightMeter read a more modest 2,048 lux for a single time-point reading in the greenhouse). However, given L. pulmonaria’s sensitivity to high UV radiation (Gauslaa and Solhaug 1999), the data gathered by the HOBO loggers suggested that the amount of sun exposure in the greenhouse might be much higher than that in the field, at least during certain portions of the day. Therefore, a shade curtain made from cheesecloth was hung around the perimeter of the frame in an attempt to protect the lichens during harsh periods of the day. Greenhouse temperatures were also measured for a 48-hour period using the HOBO Light Intensity Data Loggers, indicating an average temperature of 23°C with a maximum value of 30°C. Temperatures recorded at the collection sites of L. pulmonaria indicated an average temperature of 25°C and a maximum of 29.5°C; these values were, therefore, relatively similar. Humidity measurements for the field and greenhouse was taken using the Brunton Sherpa device and were also found to be comparable, with an average reading of 62.3% in the field and a reading of 58.4% in the greenhouse.
Boards were suspended from the frame on September 20th, 2016. Time “zero” images
(Fig. 3.3) were taken of the bark squares with each including a small section of a ruler for measurement calibration. Bark samples initially received a once-daily morning mist of distilled water using a hand-operated, plastic spray bottle. The thalli were later observed to be drying out significantly before the end of the day. This regime was, therefore, modified after roughly nine weeks to include two humidifiers (containing distilled water) set on five-minute hydration intervals every 30 minutes as well as a plastic shower curtain surrounding the frame to maximize water retention. The plastic troughs were also removed at this time to allow water vapor from the humidifiers to more effectively reach the top four boards. 67
Lichens were visited and observed roughly every other day for 12 months and were often supplemented with hand-operated misting – particularly to the upper portions of the top row of boards.
Results
After 12 months of regular monitoring, no growth was detectable in any of the treatments. Many of the propagules and even young thalli appeared to have washed off of the bark samples. Adult thalli, both injured and uninjured, had started to brown – particularly near the attachment staples and lobe tips.
Discussion
This simulation was set up to gauge whether a reintroduction of L. pulmonaria to
White Pine Hollow State Preserve might be successful. Given that no growth occurred in any of the treatments, there is no evidence indicating that a reintroduction might be successful; however, there is also no convincing evidence that a reintroduction would not be successful.
Since no growth occurred on the white cedar bark from Chippewa National Forest, a substrate that supports a robust population of L. pulmonaria in that area, it is likely that the lack of growth in this study is the result of procedural aspects or greenhouse conditions as opposed to an incompatibility of L. pulmonaria with the sugar maple bark from White Pine
Hollow. It is also possible that growth would be observed if the study were to be carried out for more than 12 months. However, similar studies with L. pulmonaria saw notable growth in
12 months or less (Scheidegger et al. 1995, Scheidegger 1995, Hallingbäck 1990). We, therefore, conclude that the tested method for the propagation of L. pulmonaria needs refinement before the approach might be useful for a reintroduction attempt. 68
One of the main issues throughout the study period was keeping the thalli adequately hydrated. As poikilohydric organisms, lichens can withstand periods of hydration and dehydration without serious detriment. However, when lichens are not hydrated, they are not photosynthesizing, which reduces their rate of growth. Having a limited timeframe to see results, keeping the treatments properly hydrated was important – though surprisingly difficult to accomplish. Another major issue was how to measure changes in growth, particularly for adult thalli controls. As the flat lobes of L. pulmonaria dry, they tend to contort and curl into themselves. Rehydrating them will more or less bring them back to their original flat, open state; however, the final shape and configuration of the lobes does not always perfectly match its previous state. This was problematic when attempting to use
ImageJ software to measure changes in surface area over time. This would likely not be as challenging to do with germinating propagules, though none were observed in this study.
Unfortunately, at the conclusion of this study, little is known as to why no growth was observed in any of the treatments. As mentioned, it could be the result of the particular method used for propagation. It is also possible that it due to some environmental aspect, which, given the final state of the adult thalli, is likely. Pesticides are used in the greenhouse and could have included compounds that are harmful to L. pulmonaria. Though the simulation was set up in a cooler area of the greenhouse, it is possible that the variation in temperature throughout the year (particularly with the inclusion of warm summer days and lack of significant seasonal temperature variation) was intolerable to L. pulmonaria and caused the lack of propagule germination and declining condition of the adult thalli. With only a limited knowledge of the growth requirements and tolerances of L. pulmonaria, it is 69 difficult to create a suitable environment for growth as well as determine why this particular environment may not have been suitable.
Though no definitive statements can be made regarding the potential success of a L. pulmonaria reintroduction to White Pine Hollow State Preserve, this study does highlight the difficulty involved in cultivating this lichen, even in controlled settings that are conducive for growth of photosynthetic organisms. Artificially created populations of L. pulmonaria would be a useful way to produce substantial quantities of individuals that could be used as material for translocations or to bolster populations in decline. The results of this study, unfortunately, suggest that producing and sustaining artificial populations of L. pulmonaria is likely to be quite challenging. Given the declining status of this lichen in North America, designing methods to increase population sizes of L. pulmonaria without putting other populations in danger, due to the harvest of translocation material, will become increasing important.
Overall, the results of this study emphasize the need for greater protection efforts of lichens, particularly those that are known to be sensitive to change, in locations where they remain present.
Literature Cited
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Figures
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Figure 3.1 Map of the replicate boards showing the randomization of the eight treatments, including those on bark from White Pine Hollow (WPH) and Chippewa National Forest (CNF). This representation is photo-documented in Figure 3.2. 75
Figure 3.2 Lobaria pulmonaria reintroduction simulation set-up. Each of the eight boards contained a representative of each of the eight treatments (see Figure 3.1).
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Figure 3.3 Treatment squares containing asexual propagules (left), young thalline lobes (center), and adult thalli (right). 77
GENERAL CONCLUSION
The purpose of this study was to develop a more complete and current inventory of the lichen diversity at White Pine Hollow State Preserve, including potentially rare or previously unreported lichens for Dubuque County and the State of Iowa. Combining the results from this study with previous data lead to an estimate of 147 lichens reported for
White Pine Hollow. Thirteen of the 117 lichens identified in this study were previously unreported for Iowa, increasing the total number of distinct lichens reported for the state to
478 from the previous estimate of 465 lichens. Seventy-two of the identified lichens were previously unreported for Dubuque County, and two had not been reported for the State of
Iowa since prior to the year 1960. Of the 71 lichens represented on algific talus slopes, 30 were collected exclusively on the slopes, including 4 of the 13 newly reported lichens.
This study also aimed to either locate extant populations of L. pulmonaria persisting at White Pine Hollow or to provide further evidence supporting its extirpation from the state.
At the conclusion of the diversity inventory of White Pine Hollow, L. pulmonaria remains unreported for the State of Iowa since 1901. Given that this lichen is large and rather obvious, it is likely that if it were persisting at White Pine Hollow, it would have been located. This survey, therefore, serves as further evidence of its likely extirpation from the state. Unfortunately, definitive conclusions cannot be made regarding why L. pulmonaria is no longer part of Iowa’s current diversity. A greenhouse experiment was constructed as a way to assess whether reintroduction efforts might be possible. Unfortunately, these attempts were unsuccessful in all treatments.
Though there is no evidence supporting the potential success of a reintroduction, there is no convincing evidence that a reintroduction would not be successful. Since no 78 growth occurred on the control substrate, it is likely that the lack of growth in this study is the result of procedural aspects or greenhouse conditions as opposed to an incompatibility of
L. pulmonaria with the bark from White Pine Hollow. However, the difficulty in propagating lichens in a controlled setting suggests that creating artificial populations of L. pulmonaria to use as material for translocations or to bolster populations in decline is likely to be challenging and potentially not feasible. It also emphasizes the need for greater protection efforts of lichens in locations where they remain present.