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Monitoring Biodiversity of San Francisco Peninsula Grasslands Using Lepidoptera As a Bioindicator Jonathan B

Monitoring Biodiversity of San Francisco Peninsula Grasslands Using Lepidoptera As a Bioindicator Jonathan B

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Fall 12-18-2015 Monitoring biodiversity of San Francisco Peninsula grasslands using as a bioindicator Jonathan B. Sifuentes-Winter University of San Francisco, [email protected]

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Recommended Citation Sifuentes-Winter, Jonathan B., "Monitoring biodiversity of San Francisco Peninsula grasslands using Lepidoptera as a bioindicator" (2015). Master's Projects and Capstones. 234. https://repository.usfca.edu/capstone/234

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This Master's Project

Monitoring biodiversity of San Francisco Peninsula grasslands using Lepidoptera as a bioindicator

by

Jonathan “Coty” Sifuentes-Winter

is submitted in partial fulfillment of the requirements for the degree of:

Master of Science in Environmental Management

at the

University of San Francisco

Submitted: Received:

...... ………...... …………. Jonathan Sifuentes-Winter Date Allison Luengen, Ph.D. Date

Table of Contents

List of Figures ...... iii

List of Tables ...... iv

Abstract ...... v

Acknowledgements ...... vi

Introduction ...... 1

San Francisco Peninsula Grasslands ...... 1

Lepidoptera in Grasslands ...... 1

Invasion ...... 2

Contemporary Integrated Pest Management ...... 4

Stability of Ecological Systems...... 6

Monitoring of Ecological Systems ...... 8

Biotic Surveys...... 8

Objective of the Paper ...... 9

Bioindicators in Natural Areas...... 11

Lepidoptera as Bioindicators ...... 12

Synthetic Herbicide ...... 16

Purpose and Controversy of Use ...... 16

Public Agency Use on the San Francisco Peninsula ...... 17

Direct Impacts to Lepidoptera ...... 20

Effects on ...... 22

Further Considerations ...... 27

Conservation Grazing ...... 28

Purpose and Controversy of Use ...... 28

Public Agency Use on the San Francisco Peninsula ...... 29

Grazing Regimes ...... 29

Direct Impacts to Lepidoptera ...... 30

Effects on Plant Community ...... 31

Further Consideration ...... 34

Prescribed Fire ...... 36

Purpose and Controversy of Use ...... 36

Public Agency Use on the San Francisco Peninsula ...... 38

Direct Impacts to Lepidoptera ...... 39

Effects on Plant Community ...... 40

Timing of Prescribed Fire ...... 41

Seeding Native Post Burn ...... 41

Recovery Time ...... 42

Further Considerations ...... 43

Further Research ...... 45

Conclusion ...... 47

Literature Cited ...... 51

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List of Figures

Figure 1: Avena barbata (slender wild oat)...... 2 Figure 2: Plant by status on the San Francisco Peninsula...... 3 Figure 3: Plant abundance by at the East Grassland of Inspiration Point, San Francisco, ...... 4 Figure 4: glaucus (blue wild rye)...... 6 Figure 5: Increased species richness increases resilience in times of drought...... 7 Figure 6: Canary in a coalmine...... 11 Figure 7: Number of listed synthetic herbicides in the Herbicide Handbook by edition...... 16 Figure 8: Lethal effects downwind from herbicide application...... 24 Figure 9: Effect of tending on survival of Hemiargus Isola (Reakirt’s blue )...... 26 Figure 10: Tule elk bugling at Point Reyes National Seashore...... 28 Figure 11: icarioides missionensis () perched on albifrons (silver lupine), its host plant...... 32

Figure 12: Hourly PM2.5 outputs during at the Yarra Valley prescribed fire event...... 37 Figure 13: Percent cover of bare ground immediately after a prescribed fire in tall grass prairie...... 40 Figure 14: Floral Resource availability to lepidoptera after a prescribed burn...... 43

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List of Tables

Table 1: Natural area protected by public agencies on the San Francisco Peninsula...... 1 Table 2: Scientific classification of and moths...... 2 Table 3: Adoption of Integrated Pest Management Programs into San Francisco Bay Area agencies...... 5 Table 4: Criteria for Lepidoptera as a biodiversity bioindicator...... 13 Table 5: Public agency herbicide policies on the San Francisco Peninsula...... 19 Table 6: Approved synthetic herbicides for use in natural areas by agency...... 20 Table 7: Ecological properties of herbicides with active ingredient in parenthesis...... 21 Table 8: Approve herbicides used in San Francisco Peninsula grasslands and their active ingredients...... 22 Table 9: Factors that influence herbicide drift...... 23 Table 10: Droplet size influences of herbicide drift parameters...... 24 Table 11: Native San Francisco Peninsula grassland species susceptibility to low rates of Roundup...... 25 Table 12: Native rhizomatous utilized by Lepidoptera in San Francisco Peninsula grasslands ...... 33 Table 13: Grazing intensity...... 34 Table 14: Common San Francisco Peninsula that have potential to be controlled by prescribe fire...... 36 Table 15: Grassland plant life form response to fire...... 41 Table 16: characteristics of integrated pest management techniques to natural areas...... 48

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Abstract San Francisco Peninsula grasslands have seen an influx of non-native invasive species starting in the 1500’s, threatening by reducing biological diversity. To combat these invasive species, multiple public agencies have begun to adopt an integrated pest management (IPM) approach. This ecologically-based approach to pest management utilizes three controversial techniques, which are presently used or are under consideration for use on the San Francisco Peninsula: herbicide application, conservation grazing, and prescribed fire. In this paper, I will evaluate the use of the taxa Lepidoptera as a bioindicator of biodiversity to assess the environmental impacts of these techniques. The application of herbicide is the most commonly used vegetation management technique evaluated. Spot spraying minimizes the direct effects to Lepidoptera, which can include reduction in number of pupae, size of adult butterflies, and wing size reduction. Unintended movement of herbicide off target is of concern. During conservation grazing with cattle, the environment must be highly managed and monitored to ensure varied sward height and heterogeneity of plant communities. Heavy grazing intensity (6.9 AMU ha-1) has large negative impacts to the environment. After a prescribed fire, plant biodiversity spikes and then declines with time while the biodiversity of Lepidoptera is inversely correlated, with recovery taking 70 months or more. As impacts to Lepidoptera from herbicide application do not disproportionately affect them, their use as a bioindicator is substantiated. This paper has found that Lepidoptera is an effective bioindicator of biodiversity for conservation grazing. Due to the disproportionate impacts to Lepidoptera during and after a fire, their ability to act as a bioindicator is not substantiated. Lepidoptera recovery time after a prescribe fire might be best utilized as a bioindicator to fire frequency. The difference in the reviewed results may be the result of the difference in disturbance characteristics that these techniques display.

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Acknowledgements I would first like to acknowledge my family, Larah, Aerowyn, and Taven, who not only made it possible for me to pursue my education, but also inspired me to care even more for that which is on loan to us from our children.

I would like to thank the following people, who took the time to answer questions and provided instrumental feedback. Liam O’Brien Liam O’Brien (local San Francisco Lepidoptera), a member of the Lepidoptera Society; Bruce Badzik (IPM Coordinator), Michael Chasse (Biologist), Alison Forrestel (Supervisory Vegetation Ecologist), and Bill Merkle (Wildlife ) from the National Park Service; Galli Basson (Resource Management Specialist) and Marisa Mibach (Open Space Technician II) from the Santa Clara Open Space Authority; and finally Cindy Roessler (Senior Resource Management Specialist) from the Midpeninsula Regional Open Space District.

Lastly, I would like to acknowledge two professors from the University of San Francisco: Dr. John Callaway and Dr. Allison Luengen. Dr. Callaway encouraged and advised me throughout my time at the University of San Francisco, giving freely to of his time to my unrelenting questions. Dr. Luengen provided invaluable guidance in the production of this paper.

We can learn about it from exceptional people of our own culture, and from other cultures less destructive than ours. I am speaking of the life of a man who knows that the world is not given by his fathers, but borrowed from his children; who has undertaken to cherish it and do it no damage, not because he is duty-bound, but because he loves the world and loves his children…

-Wendell Berry

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Introduction

San Francisco Peninsula Grasslands The grasslands on the San Francisco Peninsula (Santa Clara, San Mateo, and San Francisco counties) are considered a part of the north coastal grasslands, characterized by long lived perennial bunch grasses in a Mediterranean climate (Stromberg et al. 2004). As part of the California Floristic Province, one of twenty-five recognized botanical hotspots in the world, these coastal grasslands are known for their high biodiversity (Calsbeek et al. 2003). This uniqueness has not been lost on the highly dense urban population that lives there (Table 1). Nearly 27% of the peninsula has been set aside in perpetuity under the jurisdiction of local, regional, state, and federal agencies. These protected areas are called by multiple names, including: wildlands, natural lands, open space, preserve, refuge, or natural area. For the purpose of this paper, the term “natural area” will be used to describe these areas.

Table 1: Natural area protected by public agencies on the San Francisco Peninsula.

Population Density Protected % of Land County (people/square Area Protected1 mile)1 (square mile)2 San Francisco 17,187 9 19.1 % San Mateo 1,693 152 33.9 % Santa Clara 1,400 317 24.6 % San Francisco - 478 26.8 % Peninsula Total Sources: 1 (United State Census Bureau 2014) 2 (Orman & Voge 2015)

Lepidoptera in Grasslands The distribution of Lepidoptera (the order which contains both butterflies and moths, Table 2) is considered cosmopolitan (Learn About Butterflies 2014). Research has also shown that they are disproportionately found in grasslands and meadows, with one study showing that 52% of butterflies are found in both wet and dry meadows while this accounts for only 43% of the habitat types (Simonson et al. 2001). In addition, this study found that nearly half of the species richness (9 of a total of 19 species) were found in grasslands (Simonson et al. 2001).

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Table 2: Scientific classification of butterflies and moths. Scientific Classification Lepidoptera species utilize different grassland plants

Kingdom Animalia at different life stages by performing herbivory on host Phylum Arthropoda plants and of nectar plant. Lepidoptera species Class Insecta are known as either specialists or generalists when it comes Superorder Panorida to use of host plants (Shapiro & Manolis 2007). Specialist Order Lepidoptera Lepidoptera, such as the federally listed endangered species Icaricia icarioides missionensis (Mission blue butterfly), will lay their eggs on one or a few closely related plant species (U.S. and Wildlife Service 1984); whereas generalist Lepidoptera, such as Plebejus acmon (Acmon blue butterfly), will lay their eggs on multiple plant species within multiple plant families (Shapiro & Manolis 2007). These eggs hatch and the caterpillars will feed on the host plant (herbivory). Once caterpillars have morphed into the adult butterfly, they no longer feed but rather nectar on the , pollinating them at the same time. Vegetation community changes to both host and nectar plants can have detrimental effects on the Lepidoptera that rely on them.

Invasion Non-native plant introductions to California began in the 1500’s (Stromberg et al. 2004). By 1900, at least 34 non-native plants were introduced, largely as ornamentals, to California and are now listed by the California Invasive Species Council as having moderate or high impacts to wildlands (Stromberg et al. 2004). Other introductions were for cattle forage, erosion control, or were accidentally introduced via contamination (Stromberg et al. 2004). One such example of a grassland invader is Avena barbata (slender wild oat) (Figure 1). A. barbata outcompetes other grasses due to its allelopathic ability (a biochemical produced that negatively influences life survival of other species) and can increase fire frequency (Antonio & Figure 1: Avena barbata (slender wild oat). Picture Vitouse 1992; Medd 1996). Nearly 85% of all recovery plans used with permission, for threatened or endangered Lepidoptera species cite control of ©2014 Carol W. Witham.

2 | P a g e invasive species (LaBar & Schultz 2012). Non-native species largely do not provide the same resources or connectivity to the ecosystem as their native counterparts (Lucero et al. 2015). The small number of invasive species can have a huge impact on the ecosystem.

Plant Species Richness by Status on the San Francisco Peninsula

Non-Native, Invasive 3% Native, Not Rare 79% Non-native 6%

Native, Rare 12%

Figure 2: Plant species richness by status on the San Francisco Peninsula, data from Calflora Database 2015. Fast forward to today and we see that the plant species richness of the San Francisco Peninsula grasslands is still largely made up of native species, accounting for 91% (Figure 2). Although the native species richness is still high, the (abundance) of just 3% of the total species richness (predominately invasive non-native annual grasses) has grown to dominate many of the grassland (Stromberg et al. 2004). One such grassland on the San Francisco Peninsula is the East Grassland of Inspiration Point in the Presidio of San Francisco (Figure 3). In 2009, exotic species made up 66% of the abundance in this grassland (Presidio Trust 2015). Even after intense vegetation management over the next four years, including both invasive species removal and the out-planting of native species, the natural area still showed 49% abundance of exotic plants (Stevenson, Presidio Trust, personal communications; Presidio Trust 2015). This problem is exacerbated by the negative correlation between exotic vegetation cover and native plant richness (Beck et al. 2015). Liam O’Brien

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(local San Francisco Lepidopterist) considers invasive plants as one of the leading causes in population declines in Lepidoptera species.

Figure 3: Plant abundance by guild at the East Grassland of Inspiration Point, San Francisco, California.

Many public agencies work together though a Memorandum of Understanding and under the umbrella of a Weed Management Area working group. Weed Management Area working groups are a collective of land managers, private and public, that work together to share information, to map invasive species, and to implement projects on regionally significant invasive species (California Invasive Species Council 2015).

Contemporary Integrated Pest Management Pests are a worldwide problem, affecting many aspects of the human and natural environment. Worldwide, 40% of food crop for human use is destroyed by pests (Pimentel 2009). In an effort to control the food production environment and combat pests, humans have turned to different tools throughout time. The advent of synthetic in the 1930s quickly replaced the more traditional methods (i.e., hand removal, plowing, inorganic pesticides) within the United States of America (Pimentel 2009). As use increased in popularity and use, cautionary tales in the scientific literature began to take shape and the first precursor to an integrated pest management approach for agriculture was published (Hoskins et al. 1939). The

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University of California has defined integrated pest management as an ecologically based approach to proactively prevent or minimize the effects of pests through a variety of techniques while minimizing risks to humans, non-target species, and the environment (Universty of Califonria Agriculture and Natural Resources 2015).

Without the adoption of an integrated pest management approach, only direct cost associated with the application of pesticides are typically taken into account. Prior pest control techniques involved short term fixes which did not solve long-term problems. Indirect, external costs have been ignored, to the detriment of the human and natural environments (Pimentel 1995). To account for these externalities, an ecologically based integrated pest management paradigm has been adopted in which economics, safety, and the environment are all taken into account (Kogan 1998). By broadening the definition of pests from the agricultural setting to include those species that negatively affect natural areas, land managers could apply the broader principles of integrated pest management.

Table 3: Adoption of Integrated Pest Management Programs into San Francisco Bay Area agencies.

Natural IPM Year Plan Agency Source Area IPM Plan Coordinator was adopted (AC) Badzik, personal Golden Gate communications; 1981, Director’s National Park Skartvedt, 7,594 Yes updated in Orders Service personal 2007 communications Midpeninsula Midpeninsula Regional Open Formal Regional Open 63,000 Yes 2014 Space District Document Space District 2014a 2009, Conforti, updated in Presidio Trust personal 384 Yes Yes 2013 and communications 2015 Santa Clara Basson & Open Space Mibach, personal 15,304 No Planning N/A Authority communications

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The acceptance and implementation of integrated pest management programs into land management agencies nationwide, including the San Francisco Bay Area, has been slow (Table 3). The first known land management agency to adopt this new ecological approach in the San Francisco Bay Area was the Golden Gate National Recreation Area, a park within the National Park Service, by order of the Director of the National Park Service (1981). Conversely, Santa Clara Open Space Authority is in the early stages of the California Environmental Quality Act process for their integrated pest management program (Basson & Mibach, Santa Clara Open Space Authority, personal communications). The Santa Clara Open Space Authority does treat pests on their lands; however, the process is not systematic and treats pests on a case-by-case basis rather than on at more holistic scale (Basson & Mibach, Santa Clara Open Space Authority, personal communications). The implementation of integrated pest management will ensure the protection of the ecosystems due to the ecological approach. Stability of Ecological Systems The definition of ecological stability, also known as biotic integrity, is multifaceted (Ives & Carpenter 2007). This definition includes ideas such as the ability of populations to recover quickly after a disturbance (resilience), low variance in total over time, and consistent species richness and abundance (biodiversity) (Krebs 2008a). Although the populations of individual species may ebb and flow over time, their functional guild (i.e., the functional group occupying a similar niche), theoretically remains stable (Tilman et al. 2006). The stability of food webs is contingent upon the stability of the functional guilds that make up the (Tilman et al. 2006).

Each species within a guild typically has a slightly different life history, protecting it from certain disturbances but not others (Krebs 2008b). One example is (California oat grass), a California native perennial bunch grass. D. californica produces not only at the distal ends of stocks as typical grasses Figure 4: Elymus glaucus (blue do, but they also produce seed lower down within their wild rye), Picture used by permission, ©2015 Jean Pawek. culms, the hollow stem bearing the (Dobrenz 6 | P a g e

& Beetle 1966). This hidden seed production ability is believed to help protects its seed from herbivory (Dobrenz & Beetle 1966), but it is unable to protect itself and respond positively to fire (Hatch et al. 1999). In contrast, the California native perennial bunch grass Elymus glaucus (blue wild rye) (Figure 4) cannot withstand heavy grazing, but tolerates and responds favorably to fire (Sawyer et al. 2009). Thus, different life histories can provide competitive advantages to certain species under certain disturbances.

Low, pre-disturbance abundance of certain species can lead to extirpation (localized extinction from the area) and in the case of endangered species, possible extinction, even though guild biomass may recover from disturbances (Tilman & El Haddi 1992). Increased biodiversity contributed to increased resilience of ecological systems in times of drought (Tilman & Downing 1994). Figure 5 shows that as plant species richness increases, drought resistance (measured as the natural log of “pre-drought biomass” divided by “during drought biomass”) increases. Research plots that contained greater than five plant species returned to pre-drought biomass conditions within four years, while those with five or less species had significantly reduced biomass (Tilman & Downing 1994). The possibility of extinction is a result of guild populations being more stable while individual species population can be more volatile with Figure 5: Increased species richness increases ecosystem resilience in times of negative or positive responses depending on life drought, from Tilman & Downing 1994. history traits.

Maintaining biotic integrity of natural areas is a common management goal (Cottingham et al. 2001; Herrick et al. 2005). To meet a biotic integrity objective, monitoring is required. The National Park Service’s Inventory and Monitoring Program aims to inform natural resource planning, management, and decision making processes through vegetation inventories, including species lists, occurrences, and distribution (National Park Service 2009). The Bureau of Land Management has similar goals of inventory and monitoring and habitat management, but from

7 | P a g e the perspective of grazing and/or big game (Rich 1993). The Midpeninsula Regional Open Space District has adopted two specific monitoring goals: 1) Early Detection and Rapid Response of invasive plant species and 2) invasive species treatment monitoring (Midpeninsula Regional Open Space District 2014a). A variety of monitoring techniques are used to assess different aspects of this management goal, including vegetation cover surveys, bird point count surveys, photo-point monitoring, and bioindicators.

Monitoring of Ecological Systems Due to the complexity of ecosystems, understanding their functionality can be overwhelming at any scale (Brown et al. 2001). Despite the challenges, monitoring these systems is necessary to ensure that anthropogenic actions, or non-actions, produce the intended results and protect system constituents (108th Congress 1973). Due to these challenges, simplification of ecological systems, although not perfect, are necessary (Lomov et al. 2006). Monitoring programs need to be robust enough to inform management decisions in a meaningful way, yet not be so onerous that the monitoring costs outweigh the benefits (Noss 1990; Herrick et al. 2005).

Although monitoring efforts can range in size, scope, and complexity, most try to explain natural resources by focusing on the biota (Noss 1990; Herrick et al. 2005). To simplify the ecological environment, ecosystems have been divided into three major components to be investigated: physiochemical environment, hydrology, and the biota (Herrick et al. 2005; Mitsch & Gosselink 2007). Monitoring programs typically focus on the biotic features of the environment, as abiotic features are not only more costly to measure, but more importantly, to manipulate (Elzinga et al. 1998; Herrick et al. 2005; Ives & Carpenter 2007). Understanding the land use history, (e.g., turn of the century homestead with rangeland or an old roadbed), can guide land managers decisions to allocate funds to abiotic management if deemed necessary (Clewell et al. 2004; McGranahan et al. 2014).

Biotic Surveys Biotic surveys, which may include qualitative and/or quantitative data, assess different aspects of the environment. Survey techniques may include vegetation cover, bird count, photo- points, or bioindicators surveys. The vegetation cover surveys are used to examine the plant species biodiversity through abundance and richness of a given area (Elzinga et al. 1998;

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“Vegetation monitoring protocol” 2009). The objective of the vegetation surveys by land management agencies is typically to determine vegetation management techniques (Herrick et al. 2005). To determine habitat quality and for birds, bird point count surveys can be carried out (Ralph et al. 1995). Although bird point count surveys can be extremely important in determining the avian species richness and quality of that habitat for birds, it does not explain general trends in the ecosystem (Rowland & Vojta 2013). Photo-point monitoring can be qualitative or quantitative depending on the protocol used. Temporal changes in vegetation class (e.g., grassland to scrub) are easy to detect using repeated photographs from the same point. Vegetation class change (e.g. grassland to scrub) is easy to distinguish with time repeated photographs from the same point. Bioindicator surveys use one species or a guild of species, such as Lepidoptera, as an indication of an aspect of the ecosystem.

Objective of the Paper This paper assesses the use of species of the Lepidoptera order as a bioindicator of biodiversity within San Francisco Peninsula grasslands. This study was undertaken by analyzing the current literature on bioindicators and biodiversity within the framework of publicly protected San Francisco Peninsula grassland natural areas. Although of particular importance to human health and safety, this analysis will not consider the Wildland-Urban Interface (cities that lie within a “Fire Hazard Severity Zone,” as designated by the State of California). In addition, the Center for Biological Diversity brought a lawsuit against the United States Environmental Protection Agency for failure to protect the California red-legged from pesticides (Fimrite 2010; Center for Biological Diversity 2011). A stipulated injunction was granted on the use of certain pesticides in California red-legged frog habitat by the United States District Court (Fimrite 2010). Due to both the complexity and the unknown resolution of the litigation, this injunction will not be analyzed in this paper.

Assessment of the environment is of particular interest after vegetation treatment, especially after the use of three controversial integrated pest management techniques: application of herbicide on invasive species, conservation grazing by cattle, and prescribed fire. The effects of herbicide use, conservation grazing, and prescribed fire are investigated through this lens. Interviews with public agency personnel to determine the prevalence of these practices and potential future use by San Francisco Bay Area agencies are taken into account. San Francisco

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Bay Area experts were also interviewed to help bridge the gap between academia and practitioners. This paper will discuss the temporal and environmental criteria needed for using Lepidoptera as bioindicator and where future research is needed.

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Bioindicators in Natural Areas Bioindicators are species whose populations change due to outside influences and are seen as a reflection of the general health of the ecosystem (Holt & Miller 2010). The use of bioindicators as a monitoring technique in the environment gained considerable acceptance in the 1960’s when entomologists used historical ’ abundance data to project pest levels (McGeoch et al. 2011). Good bioindicators should reflect their environment (other taxa or an abiotic variable) and the response must be deliberate and quantifiable (Paoletti 1999; Holt & Miller 2010). Gerlach et al. (2013) characterized bioindicators into three categories based on their reflection of the environment: environmental, ecological, and biodiversity. Environmental bioindicators are generally sensitive to any change within the environment (Gerlach et al. 2013). Ecological bioindicators respond to a specific (Gerlach et al. 2013). Biodiversity indicators are correlated to other species richness and abundance (Gerlach et al. 2013). As with all monitoring techniques, the response from the bioindicator must be linked to the manipulation of the environment (Gerhardt 2002), and the choice of taxa as the indicator must be closely linked to the monitoring objective (Holt & Miller 2010; McGeoch et al. 2011).

The most famous bioindicator got its start protecting human health and safety. The real “canary in the coal mine” (Figure 6) started after the Tylorstown pit disaster of 1896 in Wales, in which the canary was an indicator to coal miners of the presence of carbon monoxide (Prior 2012). Here, a canary would show the effects of, and succumb to, carbon monoxide poisoning long before humans would recognize or have effects from the poisonous gas themselves (Wiłkomirski 2013). Taking these lessons from the past, ecologists have been using bioindicators to gauge the health and safety of the Figure 6: Canary in a coalmine. environment, not only for humans but for the rest Undated and unknown photographer. of the flora and fauna (Paoletti 1999; Gerhardt 2002).

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Contemporary use of flora and fauna as bioindicators continues for the health and safety of humans. In November of 2014, the Presidio Trust released 47 gallons of rotenone (5% solution) into a four acre lake in San Francisco, California to kill non-native fish species such as the common carp and largemouth bass (Presidio Trust 2014). The Presidio Trust used the local fish species Gasterosteus aculeatus (three-spine stickleback) as a bioindicator species, as small doses of rotenone are lethal and fast acting (McLee & Scaife 2000). Community shifts within aquatic macroinvertebrates have been used as bioindicators of increased water withdrawals (Holt & Miller 2010). have been used for air-quality bioindicators with great success (Jovan & McCune 2005). The use of bioindicators for the health and safety of the human environment has been broadened to other areas.

Scientists and land managers seek easy to use bioindicators for use in monitoring of natural areas. Gerlach et al. (2013) reviewed potential bioindicators within the class insecta due to the diversity and abundance of insects; insects are believed to be the largest of all major taxa groups. Insects encompass 53% of the known biological diversity and have the largest biomass of terrestrial according to the National Museum of Natural History. Although there is great potential for the use of insects, caution must be used as a bioindicators of biodiversity unless well-defined boundaries of the ecosystem or specific location are well defined (Gerlach et al. 2013).

Lepidoptera as Bioindicators The Lepidopteran taxa has been widely used as a bioindicator to determine anthropological effects on ecological systems (Lomov et al. 2006) due to a number of criteria (Table 4). Lepidoptera has been shown to contribute to ecosystem services by functioning as pollinators, performing herbivory, providing biodiversity, and being a food source to multiple animals such as rodents, dragonflies, lizards, birds, and bats (Bramble, Yahner & Byrnes 1997; Lomov et al. 2006; McGeoch et al. 2011). With the wide range of functions, its connections with other species, and the potential of anthropological effects on the San Francisco Peninsula, Lepidoptera will be evaluated as a bioindicator.

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Table 4: Criteria for Lepidoptera as a biodiversity bioindicator. First and second column adapted from Holt & Miller 2010, third column is from literature review.

Criteria Benchmark Literature Review (Fattorini et al. 2011; Bhardwaj Provide measurable response et al. 2012) (Hawkins & Porter 2003; Response reflects the whole Fleishman et al. 2005; Lomov Good indicator population/community/ecosystem et al. 2006; Pearman & Weber ability response 2007; Gerlach et al. 2013) Respond in proportion to the degree (Blair & Launer 1997; Bramble of contamination or degradation et al. 1997) Adequate local population density (“iNaturalist” 2015) Common, including distribution (Blair & Launer 1997; Connor Abundant and within area of question et al. 2002; “iNaturalist” 2015) common Relatively stable despite moderate climatic and environmental unknown variability (Lomov et al. 2006; McGeoch and life history well et al. 2011; Lepidopterists’ understood Society 2014) Well-studied Taxonomically well documented (Lomov et al. 2006; McGeoch and stable et al. 2011) Easy and cheap to survey (McGeoch et al. 2011) Species already being harvested for unknown Economically / other purposes commercially (Lomov et al. 2006; Public interest in or awareness of important Lepidopterists’ Society 2014; the species “iNaturalist” 2015)

Beyond the ecosystem functions, Syaripuddin et al. (2015) ranked Lepidoptera as having the most potential as a bioindicator versus bat and beetle species. This potential was based on four criteria: 1) easily identified, 2) easily surveyed, 3) broadly distributed, and 4) is indicative of diversity patterns in other groups. Substantiating the first three of four criteria, citizen scientists produced large, public data sets published on internet database such as iNaturalist (www.inaturalist.org) and eButterfly (www.e-butterfly.org). The criteria of “indicative of diversity of patterns in other groups” will be discussed further below.

Citizen science assists in meeting the requirements for Lepidoptera of the criterion of a bioindicator (Table 4). Citizen science projects have increased over the years due to growing

13 | P a g e technology and natural resource information sharing portals such as www.calflora.org, www.iNaturalist.org, and www.bugguide.net. Identification of species, and in many cases subspecies, is now possible for even the most novice naturalist (“iNaturalist” 2015). Research has shown that the identification skills of citizen scientists of hard to identify species increases with participation in citizen science projects (Kelling et al. 2015). A review of the data collected on iNaturalist (2015) shows that Lepidoptera is abundant and common in San Francisco (species richness of 267), San Mateo (species richness of 217), and Santa Clara (species richness of 95). In addition, iNaturalist has shown that there is great public interest in the taxa as a whole.

Citizen scientists work in partnership with many land agencies on the San Francisco Peninsula. “Advanced Resource Management Specialists” and “Preserve Partner” volunteers assist the Midpeninsula Regional Open Space District in both resource management as well as early detection of invasive weeds (Gartside, personal communication). Golden Gate National Recreation Area utilizes a large volunteer base to provide not only resource management, but also monitoring of rare and endangered butterflies and plant populations through highly trained interns. Resource information sharing from citizen scientists has led to an increase in available information to land managers by expanding abundance and diversity records of flora and fauna. They also can assist in data collection on specific projects of value to the land agencies. Citizen scientists receive hands-on education of the natural world and have been recognized by professional societies as essential (Lepidopterists’ Society 2014). In essence, citizen scientists have become the eyes and ears for land managers by alerting them not only to special status species, but also to invasive ones.

Another promising indication that Lepidoptera can be used as a bioindicator is the research that has shown correlations of biodiversity to other species biodiversity, meeting the good indicator criteria outlined in Table 4. The diversity and abundance of Lepidoptera has been linked to species richness in other taxa groups including birds (Fleishman et al. 2005), plants (Hawkins & Porter 2003; Lomov et al. 2006; Pearman & Weber 2007), rare plants (Simonson et al. 2001), ants (Gerlach et al. 2013), and beetles (Bhardwaj et al. 2012). Pearman and Weber (2007) also found that an increase in butterfly diversity was correlated (p<0.0001) with an increase in red-listed butterflies; species assessed by the International Union for the Conservation

14 | P a g e of Nature and considered critically endangered of becoming extinct are labeled as a red-listed species.

Research has also found correlation in butterfly abundance and species richness of the pollinator’s guild, an important ecosystem service (Pe’er & Settele 2008). In all studies, Lepidoptera was aggregated together. This is an important note, for using a narrow subsection of a taxa may skew results by distorting specific species interaction instead of looking at the general trends of the designated environment (Gerlach et al. 2013). There can be great fluctuations in population densities throughout the Lepidoptera season, showing than sampling is prone to error if not taken multiple times (Moranz et al. 2014).

As mentioned before, Gerlach (2013) cautioned against the use of Lepidoptera species as bioindicators without clearly defined ecological boundaries. Although Hawkins and Porter (2003) had reported a correlation between plant richness and butterflies at the landscape scale at the state level, they believe it is not causal but rather that plants and butterflies required the same environmental conditions to sustain their populations. What sets apart Hawkins and Porter’s (2003) correlation of butterfly and plant diversity research from other studies in California, is the scale at which the data was aggregated since most research is at a localized scale (Lomov et al. 2006; Pearman & Weber 2007). In addition, other research has shown that butterflies in subalpine meadows are not correlated to plant richness (Sharp et al. 1974), but it has also been shown that this may be due to the general trend of butterfly diversity and abundance decreasing with increased elevation (Sanchez-Rodriguez & Baz 1995).

Despite the limitations outlined above, Lepidoptera has been shown to meet the requirement of being a bioindicator of biodiversity within the San Francisco Peninsula grasslands. The taxa Lepidoptera reflects the biodiversity in many of taxa found within the natural area described, they are found to be common and abundant, well studied by both scientists and amateur naturalists within the San Francisco Bay Area, and have widespread interest of the dense urban human population. Therefore, the analysis of the use of Lepidoptera as a bioindicator of biodiversity to assess the environmental costs from three controversial integrated pest management techniques (synthetic herbicide, conservation grazing, and prescribed fire) will be examined through the rest of this paper.

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Synthetic Herbicide

Purpose and Controversy of Use In 1939, the insecticidal property of what would then become the first synthetic pesticide, dichloro-diphenyl-trichloro-ethane (also known as DDT) was discovered. Five years later, in 1944, this discovery was followed by the first known research publication about the use of the synthetic herbicide (another type of pesticide) 2,4-D dichlorophenoxyacetic, (Hamner & Tukey 1944; Carson 1962). These pesticides opened the door to an additional tool in the management of invasive species control and eradication. A quarter of a century later, 75 synthetic herbicides were in use (Bell 2015). The number of synthetic herbicides in use in the United States of America has continued to rise through the years (Figure 7). The unintended harmful effects of anthropogenic pesticides, especially DDT, as well as a wave of environmental disasters began to increase the public awareness; the publishing of Rachel Carson’s (1962) book, Silent Spring, set the stage for the controversial history of pesticide use, including herbicides.

Synthetic Herbicides in the United States 250

200

150

100

50 Weeds Science Society of America of Society Science Weeds Number of herbicides Listed by theby Listed of herbicides Number 0 1940 1950 1960 1970 1980 1990 2000 2010 2020 Year

Figure 7: Number of listed synthetic herbicides in the Herbicide Handbook by edition. Graph compiled by counting the number of herbicides listed in each edition of the Herbicide Handbook. The Herbicide Handbook is a comprehensive list of used herbicides in the United States at the time of printing. Sources: Hamner & Tukey 1944; Barrier et al. 1970; Hilton et al. 1974; Mullison et al. 1979; Beste et al. 1983; Humburg et al. 1989; Vencill et al. 2002; Senseman et al. 2007; Bell 2015.

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Concern about the widespread use of pesticide has continued today with the institutionalization of non-profit and grassroots organizations by environmental activists. The litigation over the safety of ecological systems, regardless of the human interactions, has been led by two groups: the Sierra Club and the Center for Biological Diversity. Two additional groups that inform and educate the public through both political lobbying efforts and public outreach are the Pesticide Action Network, which aims to reduce the use of pesticides worldwide, and Beyond Pesticides, which works to eliminate all pesticides. Although the concerns expressed by these groups included the safety of ecological systems, the focus is on the impacts to the human occupied environment.

In March of 2015, the International Agency for Research on Cancer classified one of most widely used pesticide in the world, glyphosate, as a “probable carcinogen” to humans (International Agency for Research on Cancer 2015). This has had immediate effects on public agencies such as the City of San Francisco due to their policy of limiting the use of probable carcinogens (Geiger, City and County of San Francisco, personal communications). Glyphosate is limited to areas that, by law, must be kept weed-free such as airport runways (Geiger, City and County of San Francisco, personal communications). The Marin Municipal Water District removed the option to use any herbicide for managing vegetation on their lands, pointing to the fact that “recent public discourse within Marin County points to a growing apprehension towards exposure to herbicides” (Marin Municipal Water District 2015).

Public Agency Use on the San Francisco Peninsula Research of herbicide effects has predominately been in the agricultural field due to the prevalent use in food production (Pimentel 2009; Gibbs et al. 2009). Loss of biodiversity has been attributed to agriculture, as it has often been cited as a main threat in many recovery plans for listed endangered and threatened species (Gibbs et al. 2009). The use of herbicide in an agricultural setting is considerably different due to application methods and the amount of herbicide used. Broadcast spraying (typical within an agricultural setting) applies herbicide to the entire site, whereas spot spraying (typical within a natural area setting) targets individual plants. Due to the nature of the application method, spot spraying minimizes the ecological impacts by lowering the rates of herbicides applied (Freemark & Boutin 1995). Additionally, the applicator can be judicial in application of herbicide to the target species with minimal off-target

17 | P a g e spray. Most research points to negative ecological effects from broadcast spraying (Freemark & Boutin 1995).

The application of herbicide on publicly held natural lands is heavily regulated at both the Federal and State levels. Implementation of the laws and regulations can vary from agency to agency due to a number of factors such as buffer zone distances (Table 5). Internal policies dictate who can apply herbicides within different land management agencies (staff, volunteers, and/or contractors). External policy by U.S. Fish and Wildlife may regulate “no spray buffer zones,” depending on the presence of special status species (LaBar & Schultz 2012). One such example is that the Golden Gate National Recreation Area is not allowed to spray within 100 feet of Lupinus albifrons (silver lupine), the host plant for an endangered butterfly (Goude 1999). “No spray buffer zones” are general in nature, rather than as a reaction to specific species response to herbicidal exposure (Dexter 1995; Bachie 2013).

There is limited data on the effects of herbicides on specific species (Freemark & Boutin 1995). The Environmental Protection Agency requires herbicide manufacturers to describe in their Material Data Safety Sheet or their Safety Data Sheet the toxicological effects on biota (U.S. Environmental Protection Agency 2015). This data is limited to describing the effects to a limited number of plants and animals. Apis mellifera (honeybee) is the lone representative for the phylum Arthropoda. Research has shown that different species can have great variability to the toxicological effects of herbicide (Freemark & Boutin 1995) and that multiple years of treatment may result in compounding negative effects (LaBar & Schultz 2012). In light of the limited data and the prevalent use among San Francisco Peninsula public agencies, the cautionary principle should be maintained as a best management practice with herbicidal application in natural areas.

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Table 5: Public agency herbicide policies on the San Francisco Peninsula. Table compiled through personal communications with agency personnel.

No Spray Buffer Zones Qualifications Agency Distance Reason(s) Staff Volunteers Contractors Direct Golden Gate  15 Feet  T&E Species supervision by National QAC or QAC or  60 Feet  Court QAC or QAL; Recreation QAL QAL Injunction Pest Control Area1  100 Feet Business License Direct Midpeninsula Direct  T&E Species supervision by Regional supervision May not  15 Feet  Court QAC or QAL; Open Space by QAC or apply Injunction Pest Control District2 QAL Business License Direct  T&E Species supervision by Presidio  20 feet QAC or May not  Surface QAC or QAL; Trust3 QAL apply  50 Feet Water Pest Control Protection Business License  T&E Species Direct Santa Clara  10 Feet  Court supervision May not Open Space  15 Feet Injunction May not apply by QAC or apply Authority4  60 Feet  Property QAL Boundary The California Department of Pesticide Regulations certifies public applicators of pesticides; QAC – Qualified Application Certificate, QAL – Qualified Applicator License. Sources: 1 – Badzik, National Park Service; Roessler, Midpeninsula Regional Open Space District; Conforti, Presidio Trust; Basson, Santa Clara Open Space Authority.

Of the three techniques analyzed, application of herbicide on plants is the most common vegetation management tool used on the San Francisco Peninsula in natural areas. Conversations with the Bruce Badzik (Integrated Pest Management Coordinator, Golden Gate National Recreation Area), Cindy Roessler (Senior Natural Resource Specialist, Midpeninsula Regional Open Space District), and Galli Basson (Resource Management Specialist, Santa Clara Open Space District) all cite the use of Roundup ProMax (active ingredient glyphosate) as the most used herbicide on public land under their jurisdiction (Table 6). After glyphosate was given the determination of “probable carcinogen” in March of 2015, the Presidio Trust’s Board of Directors moved to remove it from the list of approved herbicides (Stevenson, Presidio Trust,

19 | P a g e personal communications). The use of non-synthetic herbicides (e.g., Ecoexampt, a clover oil organic herbicide) are used infrequently by some agencies and will not be analyzed in this paper.

Table 6: Approved synthetic herbicides for use in natural areas by agency.

Public Agency

Vista

Custom

ProMax

Envoy +

Garlon 4

Telar XP Telar

Capstone Roundup

Transline

Milestone

RoundUp

Garlon 3A

Golden Gate National Recreational Area X X X X X (Badzik, personal communications) Midpeninsula Regional Open Space District (Midpeninsula Regional Open Space District X X X X X 2014a) Santa Clara Open Space Authority X X X X X X X X (Basson and Mibach, personal communications) Presidio Trust (Weed Management Guidelines: Presidio Area X X B Native Plant Community Zone 2009)

Direct Impacts to Lepidoptera Herbicide exposure to Lepidoptera is dependent on both the route of exposure and timing. Exposure may come as a result of direct contact during herbicide application, residue on plant surfaces, or ingestion during feeding and/or nectaring (Russell & Schultz 2010). Plants cannot metabolize Roundup, the most used herbicide on the San Francisco Peninsula, and the herbicide remains bioactive until the plant has decomposed (Table 7). Timing of post-emergent herbicide application can overlap with the majority of feeding and developmental period of Lepidoptera, leading to higher rates of exposure (Russell & Schultz 2010). Behavior adaptations may mitigate the effects. While diurnal Lepidoptera species are more at risk of direct exposures versus nocturnal species (Longley & Sotherton 1997), diapause behavior, such as residing in soil or thatch layers, may reduce risk to direct applications of herbicides (Glaeser & Schultz 2014).

Direct impacts due to herbicide exposure may include physiological changes in Lepidoptera species. Although each species differs in its response to direct exposure to different herbicides, common effects include: up to 32% decrease in survival rate; reduced development

20 | P a g e time, up to 10.7 ± 6.5 days earlier; 14% decrease in wing surface area; and a reduction in body weight and / or size (Russell & Schultz 2010; LaBar & Schultz 2012; Glaeser & Schultz 2014). These physiological effects reduce the fitness levels of the individual Lepidoptera and can have large effects on smaller populations (Russell & Schultz 2010; Glaeser & Schultz 2014).

Table 7: Ecological properties of herbicides with active ingredient in parenthesis. Soil persistence data is the known half-life of the herbicide. Soil types, percent moisture, solar radiation, and organic matter can influence the half-life.

# of known Soil Plant Mode of Herbicide Source Resistant Persistence Action1 Plant Species Acetyl CoA Envoy + N/A Unknown Unknown carboxylase 61 inhibitor National Garlon Pesticide 1.1 – 90 Synthetic 3 – 10 days Unknown (triclopyr) Information days auxins Center 2002 LaBar & Lipid Fusilade DX Schultz 2012; Up to 45 15 - 30 days synthesis 15 (fluazifop) Glaeser & days inhibitor Schultz 2014 Milestone Conklin & Synthetic 3 - 112 days Unknown Unknown (aminopyralid) Lym 2013 auxins LaBar & Lipid Poast Schultz 2012; 5 days Unknown synthesis 15 (sethoxydim) BASF 2014 inhibitor Amino acid Roundup U.S. Forest Not 3 - 249 days synthesis 13 (Glyphosate) Service 1997 metabolized inhibitors Acetolactate Telar Hager & More than Unknown synthase Unknown (chlorsulfuron) Nordby 2004 12 months inhibitor Valenzuela- Valenzuela, Transline Duration Synthetic Lownds & 15-287 days Unknown (clopyralid) unknown auxins Sterling 2001; Tharp 2012 1 Source: Peachey et al. 2013

Behavioral changes due to herbicide exposure have mixed results. Although butterflies did not avoid areas of sethoxydim treatment, a significantly shorter residential time was observed

21 | P a g e in both sexes (LaBar & Schultz 2012). In contrast, Glaeser & Schultz (2014) concluded that treatment with fluaziflop-p-butyl lead to increased residential time due to indirect effects to changes to vegetation. Except in the case of Icaricia icarioides fenderi (Fender’s blue butterfly, a subspecies related to the endangered Icaricia icarioides missionensis), increase in residential time did not result in an increase in oviposition (Glaeser & Schultz 2014).

Limited literature on egg deposit densities or counts by Lepidoptera suggested no impacts due to herbicidal exposure. Some species of Lepidoptera will deposit eggs higher up on host plants, and therefore are not as affected by by non-native grasses (Glaeser & Schultz 2014). Deposits of eggs higher up on the host plant also reduces the risk of exposure to herbicide application due to target application location (Glaeser & Schultz 2014). Egg deposit counts by LaBar & Schultz (2012) showed similar egg counts per plot in both the control (18.0 ± 1.8) and the grass-specific herbicide sethoxydim treatment (20.3 ± 2). Glaeser & Schultz (2014) also showed similar results for the grass specific herbicide fluazifop-p-butyl. The literature search and review did not reveal the effects of broad-spectrum herbicides and needs further research.

Effects on Plant Community Table 8: Approve herbicides used in San Francisco Peninsula grasslands and their active ingredients. Source: Senseman et al. 2007.

Active

Ingredient Vista

Custom

ProMax

Envoy +

Garlon 4 Garlon

Telar XP Telar

Roundup Roundup

Capstone

Transline

Milestone

Garlon 3A Garlon Aminopyralid X X Chlorsulfron X Clethodim X Clopyralid X Fluroxypyr X Glyphosate X X Triclopry X X X

Quantifiable effects to target plant species are known from the direct application of herbicide, but some secondary effects are unknown. Depending on the active ingredient of the herbicide and its mode of action (location where the herbicide acts on the plant species),

22 | P a g e herbicides employed in natural lands are used to create a phytotoxic (lethal) effect in the invasive plant (Table 8). Many of the herbicides applied to plants are metabolized in the plant and are rendered innocuous (Fernandez et al. 2015). The most common herbicide used, Roundup, is not metabolized (U.S. Forest Service 1997). For other herbicides, such as Milestone, their metabolism is unknown (Conklin & Lym 2013). Considering the vast majority of invasive weeds are not host plants for Lepidoptera, ingestion of herbicide from host plants should be insignificant. A major concern for land managers is unintended herbicide spray that does not make it to the target species.

Herbicide drift is the movement of herbicide away from the target plant species and is categorized as either droplet, particle, or vapor drift (Gallo 2011). Droplet drift is the most common of the three types of drift and happens when herbicide droplets are moved by the wind (Bachie 2013). Particle drift is the movement of herbicide due to evaporation (Bachie 2013). Vapor drift occurs in herbicides that are volatile with effects occurring hours after the application has been completed (Bachie 2013). Many factors may increase or decrease both the amount of herbicide and the distance traveled (Table 9). The herbicide applicator does have substantial control on the amount of drift present during an application by either adjusting application timing for proper weather conditions, including an adjuvant (an additive that improves the performance of the herbicide) in the spray mixture, or adjusting the spray equipment.

Table 9: Factors that influence herbicide drift. From Dexter 1995.

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The two largest factors that influence spray drift due to equipment is the adjustment of the aperture of the spray nozzle and the pressure within the tank (Bachie 2013). These two factors change the droplet size of the herbicide, influence the time required for deposition, and distance the drift may travel (Table 10).

Table 10: Droplet size influences of herbicide drift parameters. Table from Dexter 1995.

Non-lethal effects are typically the result of herbicide drift. Observations of a lethal dosage of herbicide were most likely to be seen within two meters downwind of the spray apparatus (Figure 8), but substantial amounts of drift can be seen up to 120 meters downwind (Marrs, Frost & Plant 1991). Non-lethal effects include reduced , growth, flower and seed production (Freemark & Boutin 1995). If the effected is the host plant for Lepidoptera, impacts (lethal or early senescence) can lower species fitness levels leading to declines in population over time (Longley & Sotherton 1997).

Shifts in community composition and physiological changes to plants may be due to low-level herbicide exposure rates (Olszyk et al. 2013). Some research has shown that Figure 8: Lethal effects downwind from herbicide application, from Marrs et al. spray drift can be more harmful to certain 1993. 24 | P a g e species than the direct spray, theorizing that non-target plants can uptake the smaller droplet size of drift more easily (Freemark & Boutin 1995). The tolerance or susceptibility of certain plants to specific herbicides can inform applicators for the need to increase cautionary measures when spraying near certain plants. There are six native plant species known to be highly susceptible to Roundup herbicide (active ingredient, glyphosate) drift in San Francisco Peninsula grasslands (Table 11). Two of these susceptible species (Elymus trachycaulus and ) are host plants for multiple grass specific Lepidoptera species (O’Brien, Lepidopterists’ Society member, personal communications). The other four species are nectar sources for many species (Shapiro & Manolis 2007). Additional, peer-review research may not have identified other plant species that are susceptible to herbicide drift yet. Although there are plants that are highly susceptible to small amounts of herbicide (1/100 of field application rate), some herbicides show different effects at low doses.

Table 11: Native San Francisco Peninsula grassland species susceptibility to low rates of Roundup. Bold species are deemed highly susceptible. Data from Olszyk et al. 2013, 2015.

% of Field Application Rate to Effect Scientific Name Common Name Height Dry Weight Bromus carinatus California brome grass 1% 10% Clarkia amoena farewell to spring 100% 100% Danthonia californica California oatgrass 1% 10% Elymus trachycaulus slender wheatgrass 1% 1% wooly sunflower 10% 10% Festuca idahoensis blue fescue 1% 1% Gilia capitata blue field gilia 1% 10% Madia elegans common madia 1% 1% Potentilla gracilis slender cinquefoil 1% 1% selfheal 1% 1% Solidago canadensis canada goldenrod 3% 3%

An unusual phenomenon that is not yet widely understood is hormesis, the positive effect of a toxic or lethal chemical when given at extremely low doses (Velini et al. 2008). Roundup (active ingredient glyphosate), the most commonly used herbicide, is one of a few herbicides that has had limited research to the hormesis effect. Sublethal application of roundup at 1 to 5 % increased biomass and reproduction in some plant species (Velini et al. 2008; Pokhrel & Karsai 2015). This suggests that herbicide drift that falls below a certain threshold, may give a competitive advantage to those species. 25 | P a g e

Buffer zones can protect sensitive areas and species from harm. As stated above, amounts of herbicide in drift drops off rapidly from the spray application site. The general consensus among researchers is that a buffer zone of 5-10m would reduce the effects of drift considerably for established perennial plants (Marrs & Frost 1997; Carlsen, Spliid & Svensmark 2006). Few significant effects to flowering or seed production and viability were found after 8 meters (Marrs & Frost 1997). Greater distances should be considered during spring in areas of high of native seedlings, as most are sensitive of up to 20 meters and some more susceptible species showing signs of damage up to 40 meters (Marrs et al. 1993).

Figure 9: Effect of tending ants on survival of Hemiargus Isola (Reakirt’s blue butterfly), figure from Weeks 2003. In addition to the direct effects to Lepidoptera and the plant community, herbicides can also effect ants that are in a mutualistic relationship with them. Myrmecophily (the term applied to the positive relationship between ants and other ) is prevalent in the family (gossamer-winged butterflies), accounting for about 75% of all species (Pierce et al. 2002). Tending ants protect Lepidopteran caterpillars from , usually by wasps, and provide a food source in return (U.S. Fish and Wildlife Service 1984; Weeks 2003). Ants can have a remarkable effect on survival rates; their presence can reduce wasp parasitization from 80% down to 40% (Figure 9). The recovery plan and the 2010 5-year review for the Icaricia icarioides missionensis (Mission blue butterfly) calls out the importance of tending ants in protecting this federally listed endangered species from wasp parasitization (U.S. Fish and Wildlife Service 1984, 2010). Vegetation can create unfavorable microclimates to species that

26 | P a g e are in mutualistic relationships with Lepidoptera; the populations of the tending ants of Lepidoptera are sensitive to both temperature and moisture changes, which are influenced by vegetation (Guiseppe et al. 2006; Glaeser & Schultz 2014). Thus, management of vegetation for tending species can benefit Lepidoptera species. Further research into the effects on other is warranted (Evans et al. 2009).

Further Considerations The use of herbicide in natural areas needs to be constrained to spot spraying. Spot spraying, by nature, is a discrete and isolated disturbance, which can be highly directed by an herbicide applicator (Dexter 1995; Wagner & Nelson 2014). Broadcast spraying is not an isolated disturbance and can lead to a disproportionate effect on Lepidoptera and the vegetation community. The long-term tracking of Lepidoptera species richness can assist in analyzing the environmental cost (i.e., loss of biodiversity) due to the use of herbicides used for treating invasive species.

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Conservation Grazing

Purpose and Controversy of Use The use of conservation grazing has come under increased scrutiny for two major reasons in California (Cohen 2015). The first is the internal disagreement between land managers and academics over the compatibility of domesticated animals grazing in an area that is to be conserved as a natural area. This internal disagreement has spilled over into the public sector such as the case at Point Reyes National Seashore. The second is the public awareness and perception of the heavy water use for cattle production.

Much is written on the use of grazing on public lands. Klitz and Miller (2015) published an article stating that grazing is a detriment to the objectives of public lands where restoration and biodiversity are important. This is due to a number of factors including lack of funding for monitoring, heavy grazing regimes, and negative wildlife interactions (Klitz & Miller 2015). Land agencies that allow conservation grazing maintain that it allows for management of fuels (for fire), increased biodiversity, supports the economy, meanwhile maintaining the rich cultural history of the area (Midpeninsula Regional Open Space District 2014b). Some research has suggested that climatic variations, such as drought, impact vegetation cover more than cattle grazing (Biondini et al. 1998).

Negative wildlife interactions have come to a head at Point Reyes National Seashore in Marin County, California. The contentious decision by the National Park Service to reintroduce Cervus canadensis nannodes (tule elk) (Figure 10) into the park in 1998, was inflamed by the already tense relationship with Figure 10: Tule elk bugling at Point local dairy ranchers (Cohen 2015). Some Reyes National Seashore. Photo by environmentalists maintain that cattle from the National Park Service. ranches have taken away forage and water resources leading to the death of 250 tule elk (Center for Biological Diversity 2015), while the ranchers maintain that the tule elk are to blame for their reduction in forage and water resources for the cattle (Cohen 2015).

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The prolonged drought in California has intensified the examination of water use by cattle. Large news outlets, such as the New York Times and National Public Radio, have run major articles in regards to this controversy, showing that livestock forage (alfalfa, pasture, and corn) is withdrawing 197 million gallons of water per day in California (Kenny et al. 2009). Estimates for gallons of water used per pound of beef in the United States range from the beef industries’ report of 441 gallons per pound (Beckett & Oltjen 1993) to “non-cattle use” advocates’ report of 12,000 gallons per pound (Pimentel et al. 2000). Despite the public perception of water use for livestock production, it only accounts for 0.60% of the 32 billion gallons of withdrawn daily, whereas irrigation accounts for 74.2% of the total (Kenny et al. 2009).

Public Agency Use on the San Francisco Peninsula Many agencies on the San Francisco Peninsula allow the use of conservation grazing on the land under their jurisdiction via lease holds to cattle ranchers. Midpeninsula Regional Open Space District grazes approximately 10,800 acres of the 63,000 acres under management, about 17%, since 2007 (Midpeninsula Regional Open Space District 2013). Other agencies that allow for conservation grazing by policy include Santa Clara Open Space Authority (Basson, personal communications), and Santa Clara County Parks (Department of Parks and Recreation & Range Managment Task Force 1992).

The two federal agencies on the San Francisco peninsula, the Presidio Trust and the National Park Service, do not use conservation grazing. The Presidio Trust does use Capra aegagrus hircus (domestic goat) as a biological control for initial removal of certain invasive weeds such as Hedera canariensis (Algerian ivy). The National Park Service does employee the use of conservation grazing at other parks (such as at Point Reyes National Seashore), but does not on the San Francisco Peninsula (Bruce Badzik, National Park Service, personal communications).

Grazing Regimes Grazing of cattle in California grasslands has the potential for both direct impacts to species in the order of Lepidoptera and indirect impacts due to change in vegetation. Grazing regimes are composed of three factors: 1) intensity of grazing, 2) season of grazing, and 3) frequency of grazing (Barry et al. 2011). All three of these factors can have disproportionate

29 | P a g e effects on both Lepidoptera and the vegetation needed to support Lepidoptera. These impacts will be qualitatively evaluated, taking the life history traits of Lepidoptera into account.

The cattle stocking rate is the product of the number of animals (using weight to standardize) and the length of time in a given area. Two common cattle standards of stocking rates exist: -Month-Unit (AMU) and Livestock-Unit. Animal-Month-Unit is used within the United States of America and equates to one cow and one calf (or a 1,000 pound animal) feeding for one month. In , the common unit is the Livestock Unit and equates to a 500 kilogram animal per hectare (Jerrentrup et al. 2014). Thus, to compare American and European research to one another, one must look take into account two separate variables. In the United States of America, the variable is the total area the cattle are gazing. Research from Europe requires examining the length of time the animals are grazing.

Direct Impacts to Lepidoptera Incidental omnivory, the unintentional consumption of Lepidoptera eggs, does lead to the susceptibility of the eggs to grazing. Baines et al. (1994) hypothesized that deer were eating eggs and larva of Lepidoptera by accident while grazing. This theory was shown in fact to be happening with another , the sheep (van Noordwijk et al. 2012). Other researchers also believe that cattle may also consume Lepidoptera accidently (Moranz et al. 2012). The location of the immobile life stages of Lepidoptera within vegetation may protect some species. Specific host plants are unpalatable to cattle, and the cattle may graze on them only if other more sought after plants have been grazed down (van Noordwijk et al. 2012). Some species of Lepidoptera go into diapause (the dormant state during development typical in insects) in the ground litter or underground completely (van Noordwijk et al. 2012). Although species that undertake diapause within the ground litter may protect it from incidental omnivory, there are other risk factors for Lepidopteran (van Noordwijk et al. 2012).

Trampling contributes to decreased survivorship of caterpillars. High intensity grazing by sheep showed a 50% decrease in survival of caterpillars with 20% of that decrease contributable to trampling (van Noordwijk et al. 2012). In contrast to high grazing, research has shown no significant difference between no grazing and low grazing on caterpillar survival rates (van Noordwijk et al. 2012). Lower grazing intensity does increase abundance of invertebrates by 35%, and this abundance only increased with accumulating years (Eschen et al. 2012). To

30 | P a g e mitigate the direct effects to Lepidoptera such as trampling, land managers will sometime exclude cattle from certain areas.

The exclusion from certain areas during grazing has the possible consequence of creating an “” where butterflies lay their eggs onto plants within the exclusion area (Farruggia et al. 2012). Once peak flower season is over, grazing is once again introduced into an area where the eggs are once again susceptible to the cattle (Farruggia et al. 2012). Once the eggs have hatched, the larva and pupae do not have a means to escape from an area which cattle may find higher in food value since it had not been grazed (Farruggia et al. 2012). Exclusion of high intensity grazing cattle during peak flowering season has been correlated to an increase in both butterfly abundance and richness (Farruggia et al. 2012).

Effects on Plant Community As discussed in the San Francisco Peninsula Grassland section, invasive species have taken a strong hold. Beck et al. (2015) showed that without intervention, ungrazed areas have seen a significant loss of plant species richness over time (4.5 ± 0.78 species lost over 3 years) versus grazed areas (0.5 ± 1.32 species gained over 3 years) in California grasslands. Countering this general trend was Kruess & Tscharntke (2014) showing that ungrazed areas have a greater species richness of bees, wasps, and butterflies; this study was conducted in Germany and the results may be not applicable to San Francisco Peninsula due to the very different climatic conditions between study locations. Climatic variation has been shown to change vegetation cover more than cattle grazing (Biondini et al. 1998).

The use of cattle grazing has decreased the exotic grass cover over time (22% ± 5.6%) versus ungrazed areas in which the cover increased (13.8 % ± 11.64%) (Stahlheber & D’Antonio 2013; Beck et al. 2015). As the percent cover of exotic grass decreased, native plant richness increased (Beck et al. 2015). Beck et al. (2015) hypothesized that the native plant seed bank was still present leading to this increase. It has been theorized that the increase in exotic grass has led to the decrease in population of forb host specific butterflies, such as the Icaricia icarioides missionensis (Mission blue butterfly, Figure 11) by Bill Merkle (Wildlife Ecologist, National Park Service) due to butterflies not being able to locate host plants overgrown by the exotic grasses. The reduction in exotic grasses using cattle within the confines of conservation grazing may assist in the recovery or maintenance of forb hosting butterfly species.

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The effect on forbs, mentioned above, indicates that land managers need to understand the vegetation composition of the pasture. Prior to allowing cattle into natural areas, land managers need to understand the possible response of the vegetation present. Pre-existing native plant cover is associated with butterflies after treatments (Moranz et al. 2012). Yearly monitoring needs to be in effect Figure 11: Icaricia icarioides missionensis because grazing is not a significant factor (Mission blue butterfly) perched on Lupinus in the change of abundance in native forb albifrons (silver lupine), its host plant. Photograph ©2014 Jonathan Sifuentes-Winter. cover until multiple years of grazing has been implemented (Stahlheber & D’Antonio 2013; Beck et al. 2015). Pretreatment conditions may require native plant restoration due to historic land use and the abundance of native and exotic forbs that are present (Moranz et al. 2012). Depending on pretreatment conditions, supplementing the native seed banks may also be necessary (Moranz et al. 2012).

High intensity grazing disturbs -plant interactions (Kruess & Tscharntke 2014). One common California perennial grass that reproduces by is (red fescue), the host plant for colorado dodgei (Dodge’s butterfly) (Shapiro & Manolis 2007). Skipper butterflies host on grasses and many are thought to host specifically on F. rubra as well (O’Brien, Lepidopterists’ Society member, personal communications). As Table 12 shows, host plants are only one reason to be concerned about the effect on the rhizomes of plants as they are also nectar sources for adult butterflies.

Cattle grazing can also lead to effects on forbs as well. Grazing has been shown to support short statured species, such as forbs with basal rosettes (Stahlheber & D’Antonio 2013). Stahlheber & D’Antonio (2013) also noted that forbs increased with cattle, but that was true for exotic as well as native species. Hayes and Holl (2003) saw in their research that coastal grasslands had a possible increase in native annual forbs with a decrease in native perennial forbs. Exotic forbs that have naturalized in California may be the species that are the most

32 | P a g e tolerate of grazing, whereas California native forbs have varied adaptations to disturbances (Stahlheber & D’Antonio 2013).

Table 12: Native rhizomatous plants utilized by Lepidoptera in San Francisco Peninsula grasslands. Common names provided based off the Calflora Database.

Scientific Name1 Common Name1 Host2 Nectar Source3 painted lady common yarrow many millefolium butterfly skippers, moths, Anaphalis pearly everlasting American painted margaritacea butterfly lady butterfly Artemisia California American painted unknown douglasiana mugwort lady Asclepias narrow monarch many fascicularis milkweed Cardamine mustard white milkmaid unknown californica butterfly Festuca rubra red fescue Dodger’s skipper unknown west coast lady, painted Heterotheca lady, checkerspots, false goldenaster unknown sessiliflora gray hairstreak, cabbage white, coppers Leymus triticoides creeping wildrye woodland skipper unknown northern Symphyotrichum checkerspot, field Pacific aster many chilense crescent, pearl crescent Sources: 1 Calflora Database, 2 Shapiro & Manolis 2007, 3 Caldwell 2015

Long-term heavy intensity of grazing leads to long-term impacts to the environment. These impacts include changes to species composition, plant biomass, plant physiological changes, and nutrient cycling (Biondini et al. 1998). Stocking rates of 6.9 AMU per hectare on average remove 75% of the forage (grass) in an area, leaving less than 500 pounds of residual dry matter (amount of plant material left behind after grazing) at the end of the grazing season (Table 13). Midpeninsula Regional Open Space District uses 800 to 1,200 pounds of residual dry matter as the target goal for their pastures, equating to a moderate to conservative stocking level (Koopmann, Midpeninsula Regional Open Space District, personal communications). Residual dry matter influences many aspects of the biotic environment, including the next years species composition (Bartolome, Frost & McDougald 2002).

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Table 13: Grazing intensity, based on Barry et al. 2011 and Dong et al. 2013.

Non-Use Stocking (or insignificant Light Conservative Moderate Heavy Level use) Forage Insignificant 25% 50% 50-75% > 75% Removal Varies due to 1,500- Residual 1,000-1,500 500-1,000 < 500 past year 2000 Dry Matter pounds pounds pounds accumulation pounds Animal 2.7 AUM 6.9 AUM - - - Units ha-1 ha-1

Heavy grazing would negatively impact many California perennial grasses and forbs that vegetatively reproduce via rhizomes (Stromberg et al. 2004, Table 12). Decrease in production is a plants physiological change due to heavy grazing (Dong et al. 2013). Rhizomes not only offer a way to increase population of species through vegetative reproduction, but also store energy to be utilized by plants during the next years growing season (Janeček & Klimešová 2014). The reduction in rhizome production would leave this species vulnerable to competition by other plants.

Decreasing grazing intensity has additional benefits to the environment. Abundance of butterflies is affected by the sward height (i.e. plant heights within the field) and composition of dissimilar species (heterogeneity), along with the diversity of nectar species (Jerrentrup et al. 2014). An irregular vegetation height structure in grasslands will protect biodiversity by providing different niches for different species (Jerrentrup et al. 2014). Thus, ecological stability of native forbs, plant diversity, and plant richness is increased in response to a lower grazing intensity (Beck et al. 2015).

Further Consideration Land managers must closely monitor and manipulate the grazing regime for cattle to be effective in the conservation of natural areas. Pastures must be small enough that the cattle graze the entire site, as large pasture can create areas of congregation around preferred food and water sources (Barry et al. 2011). The need for increased monitoring and management intervention will increase costs to the public agencies charged with protecting and enhancing the natural area. The use of Lepidoptera as a bioindicator of biodiversity cannot be used alone, but rather should

34 | P a g e supplement a robust rangeland monitoring protocol, including identification of at-risk areas and soil issues (i.e., bare ground or high erosion areas) (Veblen et al. 2014).

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Prescribed Fire

Purpose and Controversy of Use Prescribed fire has become a conventional management tool in grassland maintenance (Reiner 2007). The technique has come into greater use due to the ecological scale at which it can be applied. A number of ecological benefits result in the use of fire, including: 1) a reduction in fuel levels that can lower wild fire intensities, 2) a decrease soil nitrogen loads caused by nitrogen deposition, 3) maintaining grasslands by removing encroaching scrub, and 4) control of invasive plant species at a landscape level (Alexander & Antonio 2003; Reiner 2007). Prescribed fire has the ability to manage multiple invasive species on the San Francisco Peninsula (Table 14).

Table 14: Common San Francisco Peninsula invasive species that have potential to be controlled by prescribed fire.

Common Special Scientific Name Literature Review Name Considerations Incomplete burns will Sweet et al. 2008; Aegilops sp. goat grass require a second burn Marty et al. 2015 the following year. Avena barbata, A. fatua, Bromus diandrus, B. Abundance returned to exotic annual hordeaceus, B. Dickens et al. 2008 pre-burn conditions grasses madritensis ssp. rubens, within 4 years. Festuca myuros Requires three years of yellow star Centaurea solstitialis DiTomaso et al. 2006 prescribed burns to thistle control. Alexander & Antonio Hand pulling may be Cytisus scoparius Scotch broom 2003 more effective. Requires high biomass medusahead Kyser et al. 2008; Elymus caput-medusea of other grasses for grass Sweet et al. 2008 greater fire intensity. Reduced seed bank, original plants re- Festuca arundinacea tall fescue Emery et al. 2011 sprouted. Follow up required. Alexander & Antonio Hand pulling may be Genista monspessulana French broom 2003 more effective.

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In May of 2000, 235 homes were destroyed and well over 18,000 people were evacuated from the Los Alamos, New Mexico area due to a escaped prescribed fire set by the National Park Service (Holloway 2000). A review of prescribed fires in 2012 showed that 14 prescribed fires (of over 16,600) escaped United States wide (Wildland Fire Lessons Learned Center 2013). Of these escaped prescribed fires, ten were set by federal agencies, three by States, and one was private. Although these 14 fires comprised only 0.08% of all prescribed fires, they have lasting negative effects on the public perception of agencies abilities to perform their duties in a safe and effective way (Brunson & Evans 2005).

Figure 12: Hourly PM2.5 outputs during at the Yarra Valley prescribed fire event. Dash line shows the advisory 24-hour NEPM standard (Haikerwal et al. 2015). The use of prescribed fire has also been under scrutiny for contributing to air of the surrounding areas, which negatively effects human heath (Boxall 2000). The health impact to humans is due to the fine particulate matter (PM2.5) that is released by the fire which is above the National Environmental Protection Measures (NEMP) standards (Haikerwal et al. 2015, Figure 12). Increases in pulmonary diseases and doctor related interventions have been widely established as results of increased PM2.5 levels (Haikerwal et al. 2015). This has led to increased opposition to the use of prescribed fire near heavily populated areas.

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Complementing this increased public opposition, regulatory agencies monitor land management agencies for the public good. On the San Francisco Peninsula, the Bay Area Air Quality Management District issues permits for prescribed fires and fines agencies and individuals that burn outside of the permit conditions. In 2011, Golden Gate National Recreation Area was fined for the Gerbode Prescribed Fire, initiated for the control of the invasive grass Festuca arundinacea (tall fescue), for producing heavy amount of smoke that settled on the city of Sausalito, California (Bay Area Air Quality Management District 2012).

Public Agency Use on the San Francisco Peninsula The use of fire as a land management tool on the San Francisco Peninsula falls under one of two techniques: flaming and prescribed fire. Flaming is the use of a portable torch, fueled by propane, applied to specific plant species to kill it. Application of flaming requires the use of at least two personnel, the applicator and safety point person. Although applications of flaming are done under strict weather prescriptions, it is not considered a prescribed fire due to its narrow scope and precision of application. All interviewed public agencies allow for the use of flaming on its jurisdictional lands. Prescribed fire, also done under strict weather conditions, is used for multiple purposes including fuel reduction and habitat restoration (Stromberg et al. 2004). Application of a prescribed burn requires a great deal of planning and pre-burn treatments (creation of fire lines to contain the fire). The day of a prescribed fire can require a great number of personnel depending on the prescription and burn area.

Two agencies on the Peninsula allow the use of prescribed fire: Santa Clara County Parks and Golden Gate National Recreation Area. The minimization of prescribed fires in these two parks is due in part to the proximity of a dense urban population and the potential impacts to the human environment, such as the case with Golden Gate National Recreation Area’s Gerbode Prescribed Fire. Two additional agencies, Santa Clara Open Space Authority and Midpeninsula Regional Open Space District, are in the beginning phases of writing Fire Management Plans that will evaluate the use of prescribed fire for fuel reductions, habitat restoration, and training opportunities for area staff for wildland fires (Basson & Mibach, Santa Clara Open Space Authority, personal communications; Roessler, Midpeninsula Regional Open Space District, personal communications). The Presidio Trust does not allow the use of prescribed fires (Conforti, Presidio Trust, personal communications).

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Direct Impacts to Lepidoptera Negative direct impacts to Lepidoptera from fire are weighted towards the immature stages (i.e., eggs, larva, and pupa) because they are less mobile or immobile. Moranze et al. (2014) saw that the Speyeria idalia (regal butterfly), a grassland obligate butterfly of mid-west United States, stayed above ground during it immature stages and thus all were killed due to a winter prescribed fire. There are few individual adaptations of larvae or pupa to escape the effects of fire: hypogeal larvae (which reside within the soil) in addition to the avoidance of ovipositing adults of more fire prone areas.

There are a few species of Lepidoptera larvae, mostly moths, which are protected from the effects of prescribed fire due to their hypogeal (living below ground) behavior. Regardless of the fire intensity, below ground biology is protected from fire due to the insulating characteristics of soil and the moisture found within (Bradstock & Auld 1995). One native species to San Francsico Peninsula that does have hypogeal larvae is the Hepialus californicus (ghost moth) (Strong et al. 1995). Prescribed fire would not directly affect species with hypogeal larvae, but the change in vegetation composition could have indirect impacts as discussed below.

Some species of Lepidoptera avoid fire prone areas during egg laying. As an example, the European butterfly fagi (woodland grayling) deposits eggs on grasses in sparsely vegetative areas (Möllenbeck et al. 2009). As mentioned in the conservation grazing section, it is theorized that the decrease in population of Icaricia icarioides missionensis may be contributed to invasive annual grasses concealing its host plants (Merkle, National Park Service, personal communications). The principle host plant of I. acarioides missionensis is Lupinus albrifrons var. collinus (silver lupine), a plant species that does well in rockslide disturbances (U.S. Fish and Wildlife Service 1984). Few other native species of the San Francisco Peninsula respond quickly to such a disturbance, leaving the area sparsely vegetated for a short time (Chasse, National Park Service, personal communications; Forrestel, National Park Service, personal communications). It is possible that I. acarioides missionensis seeks out sparse vegetation as well and thus its immature stages may have been protected in the past during fire, prior to the invasion of non-native annual grasses.

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Effects on Plant Community Fire has an immediate effect on the above ground vegetation and thatch layer. Combustion of vegetation material is dependent on many factors that include amount and type of biomass (fuel type), weather conditions, and topography (Weir 2009a). To determine the appropriate frequency of prescribed fire, land managers needs to take into account grass thatch build up, as this is a driving force of species richness decline (Twidwell et al. 2012). Immediately after a fire, percent cover of bare ground can increase dramatically (Weir 2009b; Vogel et al. 2010). Figure 13 shows that it can take approximately 42 Figure 13: Percent cover of bare ground immediately after a prescribed fire in months after a prescribed fire for the percent tall grass prairie, from Vogel et al. 2010. cover of bare ground to return to pre-burn As germinate, vegetation re- sprouts, and thatch accumulates, the conditions. This change is due to increased plant amount of bare ground decreases with biomass and grass thatch accumulation over time. time.

The response of vegetation after the fire depends on the response of the individual species and their adaptions that the plant has developed over time (Simmons et al. 2007). As a guild, native forb richness increased in extreme fire, but individual species had different responses (Twidwell et al. 2012). Many plants have adapted to fire through physiological changes to root structures or seed, while other non-adapted species are left at a competitive disadvantage (such as annual species) (Table 15). Fire adapted species will have one or more of the following characteristics: rhizome production, apical meristems (growth point) located below the ground surface, hard coated seeds, or seed that is buried into the soil (DiTomaso et al. 2006). As with cattle grazing, plants with protected growth tissue will respond with new growth (DiTomaso et al. 2006).

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Table 15: Grassland plant life form response to fire, from DiTomaso et al. 2006.

Timing of Prescribed Fire The timing of prescribed fire to control invasive species must be precise. Seeds of three common exotic grasses to the San Francisco Peninsula (Aegilops sp. - goat grass, Elymus caput- medusae - medusa head, and Bromus diandrus - ripgut brome) show low susceptibility to fire when present on the soil, but higher susceptibility to direct flames when seeds are still attached to the plant (Sweet et al. 2008). Thus it is recommended to time prescribed fire prior to seed drop to insure higher fuel loads and to increase exposure time to seed (Sweet et al. 2008). Most happen during the summer months, while prescribed fires happen during the spring. Research has shown that effects to growth buds on grasses respond differently depending on the season and varies by species (Russell et al. 2015). Prescribed fire for invasive species control could have unintended vegetative effects beyond the control of the target species.

Seeding Native Species Post Burn Seeding into a burned area with native seed provides limited benefits. A common misconception is that the establishment of native grasses will compete with and decrease the percent cover of non-native invasive annual grasses. Research by Busby & Southworth (2014) showed that percent cover did not decrease by the presence of greater cover of native species (Busby & Southworth 2014). Exacerbating the situation, persistence of native

41 | P a g e bunch grasses fell sharply after seven years with no additional management, from 10% cover in year 2 to 2% in year 7 (Busby & Southworth 2014).

Recovery Time Presumption of recovery time by land managers needs to be reevaluated for Lepidoptera. Recovery time is the amount of time it takes for taxa to meet the same level of abundance and richness after a disturbance, in this case a prescribed fire. Prairie specialist species have been presumed to recover in no more than five years, but Vogel et al. (2010) showed that habitat- specialist butterfly’s richness recovery time was greater than 70 months and abundance took 50 months to fully recover in some grasslands. Increasing the frequency of burns to every 2 to 6 years has shown marked declines in specialist butterflies (Swengel & Swengel 2015). If the prescribed fire is for land management of individual prairie specialists (such as endangered species), they may need species-specific management plans (Swengel et al. 2011). Recovery time is influenced by three main factors: 1) distance of unburned vegetation similar to pre-burned vegetation, 2) burned vegetation is suitable for recolonization, and 3) time lapse between disturbances (Moranz et al. 2014).

Flying distance of Lepidoptera species also influences recovery time. Unburned vegetation similar to that of the pre-burned vegetation within flying distance is likely to contain a reserve of unaffected Lepidoptera. Flying distance varies greatly among Lepidoptera. The endangered Icaricia icarioides missionensis (Mission blue butterfly) typically moves no more than 64 meters and has a maximum flight distance of 2,500 meters, while the Callophrys mossii bayensis (San Bruno Elfin) typically moves less than 100 meters and no more than 800 meters (U.S. Fish and Wildlife Service 1984). In Moranz et al. (2012) study, they attributed the quick recovery time of two prairie specialists (Cercyonis pegala and Speyeria idalia) to unburnt grasslands that were within 500 meters from burned boundaries of all their study sites.

Recovery time is an important management consideration when determining fire return intervals (frequency). Historical fire frequency on grasslands by native Americans were very frequent, with some areas burned on an annual basis (Aschmann 1977). Grasslands that are under a burn plan in the present day are typically treated on a one to five year rotation (Moranz et al. 2014). Considering that the S. idalia recovery was within the first summer after the fire to pre-burn populations sizes, some could conclude that a five year rotation is sufficient (Moranz et

42 | P a g e al. 2014). Moranz et al. (2012) believes that this quick recolonization was due in large part to unburned grasslands near the burn treatment areas, as two prairie specialist showed no signs of population decrease after a March prescribed fire. Long term fire management can increase height and thickness of perennial grasses, which has shown to decrease biodiversity (Swengel & Swengel 2015).

Weather conditions have limited effects on the response of vegetation to prescribed fire. Weather parameters (the prescribed fire prescription) dictates whether a prescribe fire may be initiated or if the agency must stand-down from ignition (Weir 2009c). Extreme fire behavior caused by drought and during the growing season in coastal prairie does not decrease the native plant richness in the burned area (Twidwell et al. 2012). Weather conditions can affect the overall burn completeness within an area, leaving some areas of unburned vegetation (Wildland Fire Lessons Learned Center 2013). These areas of unburned vegetation can acts as refugia for other species.

Further Considerations The use of Lepidoptera as bioindicators of biodiversity does have limitations for prescribed fires. Recovery time for Lepidoptera species richness and abundance increases with time, but the plant species richness increase is short-lived and decreases with time since burn (Twidwell et al. 2012, Figure 14). Concurrent with the short-lived increase in species richness is the short-lived increase in floral resources (number of flowering stems). As stated before, grass litter buildup is negatively correlated with plant species richness (Twidwell et al. 2012). These opposing trends appear to contradict the possible use of Lepidoptera Figure 14: Floral Resource species richness and abundance as a bioindicator of availability to lepidoptera after a prescribed burn, from Vogel et al. biodiversity for prescribed fire in the initial years, at least 2010. for plant biodiversity. Recovery time for Lepidoptera could possibly be used as an ecological bioindicator for fire frequency.

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The burning of entire grasslands can have devastating effects on slow moving biota, especially if the grassland is isolated or small in nature. Burning entire grasslands that are isolated has extirpated grassland obligate species in the past (Swengel et al. 2011). Fire size may play a role in the ability of Lepidoptera to increase in population as a smaller site may in fact be more prone to extirpation as well (Moranz et al. 2014). In burned areas that bordered unburned areas, higher populations of Lepidoptera were seen (Moranz et al. 2014). In addition, higher populations were seen in the burned areas compared to unburned areas during the next year, an indication of short distance migration (Moranz et al. 2014). This migration is contributed to forbs’, a nectar source for the butterfly, positive response to fire by increasing in both population numbers and floral resources (Moranz et al. 2014). Recovery of the grassland obligate butterfly, S. idalia (considered to be a strong flier) was within the first summer after the fire to pre-burn populations due to quick recolonization from other nearby areas (Moranz et al. 2014).

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Further Research The analysis of three controversial techniques used on the San Francisco Peninsula grasslands did not take into account three important considerations: 1) Wildland-Urban Interface, 2) aquatic features, or 3) threatened and endangered species (including their critical habitat designation). Encumbered by a substantial amount of Federal, State and local laws, regulations, and court orders, these three considerations were outside the scope of this analysis. The following suggested research will increase the awareness of impacts on natural areas and the human environment.

Cities that are within a state designated “Fire Hazard Severity Zone” are considered to be within the Wildland-Urban Interface (State of California 2007). Increased awareness of the impacts to the human environment in these zones requires a greater analysis. Impacts may include not only the effects of human health due to prescribed fire (as discussed in the prescribed fire controversy section of these paper), but also the increased fire severity if fuel loads are not properly managed.

Land managers must also take into consideration impacts to aquatic features due to vegetation management. Midpeninsula Regional Open Space District defines an aquatic feature as “any natural or manmade lake, pond, river, creek, drainage way, ditch, spring, saturated soils, or similar feature that holds water at the time of treatment or typically becomes inundated during winter rains” (Midpeninsula Regional Open Space District 2014a). Additional permits, mitigation measures, and monitoring may be required to ensure the safety of the aquatic environment. Compliance with and implementation of the Clean Water Act includes, most notably, Section 401 ( Certification) and Section 404 (discharge, dredging, or fill into the waters of the United States). The analysis of impacts due to cattle may include increased erosion and/or nutrient levels (due to manure) into aquatic features.

Threatened and Endangered species are critical to biodiversity and require special consideration anytime human activity may affect them, including the application of any vegetation management technique (108th Congress 1973). These species vulnerable to extinction are listed by the Secretary of the Interior under the authority of the Endangered Species Act of 1973. Of the 292 species listed in California, four are butterflies on the San Francisco Peninsula: Callophrys mossii bavensis (San Bruno elfin), Euphydryas editha bavensis

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(bay checkerspot), Icaricia icarioides missionensis (Mission blue butterfly), and Speyeria callippe callipe (Callippe silverspot) (U.S. Fish and Wildlife Service 2015). Increases in pesticide use on arable farmlands has become a conservation concern for these species (Freemark & Boutin 1995). Understanding and analyzing the life history of threatened and endangered species and the impacts of management is vital to the stability and recovery of the listed species, and biodiversity as a whole.

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Conclusion Integrated pest management for invasive species by public agencies on the San Francisco Peninsula needs to be assessed to determine the environmental impacts due to vegetation management and to ensure that externalities are accounted for. The use of synthetic herbicide, conservation grazing, and prescribed fire are of particular concern due to a number of factors, including the controversial nature of each of these techniques. Additionally, multiple treatments are usually necessary to kill target invasive species leading to the possibilities of cumulative impacts over time (Stanley, Kaye & Dunwiddie 2011). To assess these techniques and their impacts to biodiversity, this paper examined the use of the taxa Lepidoptera as a bioindicator.

Lepidoptera’s biodiversity, both species abundance and especially species richness, has been linked to the biodiversity of multiple other taxa groups, including other insects, mammals, reptiles, birds, and plants. The correlation of Lepidoptera biodiversity is increased by the three other criteria for bioindicators, they are: 1) abundant and common in grasslands, 2) well studied by both the professional and amateur scientists through the Lepidopterist Society and other citizen science projects, and 3) the public at large is interested in their conservation. According to this literature review, as long as the monitoring of Lepidoptera is performed at an appropriate scale, within the confines of San Francisco Peninsula grasslands, and over the entire temporal span of the monitoring season, Lepidoptera biodiversity will provide an indication of the overall biodiversity of the ecosystem.

Although there is little research on specific tolerance and susceptibility levels of specific species and herbicides, the unanimous consensus of public agency personnel is that herbicide use is a necessary tool to combat invasive species. Using qualified herbicide applicators who understand the life histories of not only the target plant species, but also that of non-target species, will reduce the effects of herbicide drift. Unlike the other two integrated pest management techniques, herbicide application in natural areas can be considered a small, discrete disturbance to the area with little risk of disproportionate impacts to Lepidoptera versus the environment as a whole. Thus, monitoring Lepidoptera biodiversity will increase our understanding of the impacts of herbicide to the ecosystem as a whole, and how the biota responds to those impacts.

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Consistent monitoring of conservation grazing using cattle is required to manipulate the grazing regime, protecting the natural area from overgrazing (Veblen et al. 2014). The use of Lepidoptera as a bioindicator is an appropriate additional monitoring scheme, but should not be used in isolation. Overgrazing can quickly increase or hasten detrimental soil conditions due to erosion in which Lepidoptera monitoring would not be able to capture in a timely matter (Herrick et al. 2005).

As described in the bioindicator section of this paper, Gerlach et al. (2013) categorized three different types of bioindicators (environmental, ecological, and biodiversity). The literature reviewed for this paper did not substantiate the use of Lepidoptera as a bioindicator for assessing biodiversity post prescribed fire treatment due to the disproportionate impacts to the taxa versus plant populations. Plant biodiversity was negatively correlated with Lepidoptera biodiversity over time (Twidwell et al. 2012). Mitigation by supplementing the natural area with native plant seeds had limited benefits that dissipate within seven years (Busby & Southworth 2014). However, using Lepidoptera after prescribed fire as an ecological bioindicator is more appropriate and could be used to signal ecosystem recovery time.

Table 16: Disturbance characteristics of integrated pest management techniques to natural areas. Differences in characteristics are due to the nature of the integrated pest management techniques.

Integrated Pest Landscape Human Ability Major Disturbance Management Disturbance to Change Influence Time Technique Type Disturbance Synthetic Weather / Discrete Isolated High Herbicide1 Equipment Conservation Continuous / Stocking Rate Mosaic Medium Grazing2 Seasonal Prescribed Weather / Discrete Continuous Low Fire3 Topography Source: 1 Dexter 1995; 2 Herrick et al. 2005; Koopmann, Midpeninsula Regional Open Space District, personal communications; 3 Weir 2009a.

The three integrated pest management techniques researched in this paper had distinct differences in their application to the natural area. Although synthetic herbicide and prescribed fire are both a disturbance that has a discrete time frame, the landscape disturbance type is quite different (Table 16). Spot spraying within the landscape are isolated disturbances versus the

48 | P a g e continuous nature of fire. These inherent differences in disturbance characteristics may explain the results of the inconsistent ability to use Lepidoptera as a bioindicator for biodiversity.

Treatment of invasive species requires a truly integrated approach; not only does an integrated approach insure the control of the species, but it also makes sure that the costs to the environment have been fully accounted for. Depending on the target species, additional techniques that do not have such wide spread effects should be considered as well, such as solarization, mowing, or manual removal. In addition, proactive approaches can be incorporated into habitat restoration activities that can include seeding of native species, an early detection/rapid response protocol, and increased educational opportunities for the visiting public and management staff about the spread of invasive species.

In the fight against invasive species, we should reexamine the assumption that vegetation management is always required. Higher environmental impact techniques may require a time of no management to let the ecosystem recover. Rotating impacted areas, no matter the vegetation management treatment method, will act as refugia for species that are more sensitive to certain treatment methods and should allow for the recovery of those species (Swengel et al. 2011; LaBar & Schultz 2012). As discussed, individual species have specific life history traits that may allow for resilience in the face of one disturbance but not another (McGeoch et al. 2011). Individual species within the same guild collectively contribute to ecosystem resilience and thus, the conservation of biodiversity. Rotational management when using higher environmental impact techniques may allow for the recovery of non-target species.

The implementation of the three controversial techniques analyzed must be made on a case-by-case basis. Additional management goals (i.e., fuels reduction for potential wildland fire), the target invasive species, and non-target species presence all play into the decision to use one technique over another. As discussed, each vegetation management technique has the potential to assist in the recovery an invaded ecosystem when used properly. An interdisciplinary team is typically able to engender the required knowledge of the natural area to make the decision of how best to treat particular invasive species.

San Francisco Peninsula grasslands provide a large portion of the species richness of the California Floristic Province, accounting for 22% of the known species occurring there (“Calflora Database” 2015). Efforts to maintain this biological hotspot must be evaluated to

49 | P a g e ensure that objectives are met with the lowest environmental costs possible. Only through an ecologically based approach to vegetation management (i.e., integrated pest management) are all costs accounted for. Public agencies and their employees have been entrusted with protecting these natural areas using the best available science. This paper demonstrated that the use of Lepidoptera as a bioindicator for biodiversity will assist land managers in ensuring that this trust will not be misplaced.

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