Journal of Zoological Research | Volume 02 | Issue 03 | July 2020

Journal of Zoological Research http://ojs.bilpublishing.com/index.php/jzr

ARTICLE Butterfly Diversity on a Southeast Florida Military Base Located within an Urban Matrix

Sandy Koi1* Craig van der Heiden2 1. Conservation Associate, Entomology, Institute for Regional Conservation, 100 E. Linton Blvd., Suite 302B, Delray Beach, Florida, 33483, USA 2. 5800 S.W. 188 Avenue, Southwest Ranches, FL, 33332, USA

ARTICLE INFO ABSTRACT

Article history South Florida is a renowned ‘hotspot’ for rare and endemic taxa, with Received: 30 June 2020 and plants found in few other ecosystems. Specialized species evolved in Florida’s stochastic climate, adapting to seasonal drought Accepted: 14 July 2020 and flooding, hurricanes and high-wind tropical storms. As human Published Online: 20 August 2020 population growth and development increased, and natural ecosystems disappeared, or became increasingly degraded, at-risk taxa now face Keywords: additional threats, such as urban pesticide use and fragmented remnant Air Force habitats. The ability of species to adapt to these changing ecological factors is one of the dynamics that either impacts their fitness to greater Butterflies survival or drives extirpation or extinction. Butterflies are native indi- Habitat alteration cator species that can be used to document environmental conditions Invertebrates affecting many other taxa. Butterfly surveys were conducted over 16 months on an active military air reserve base located within a mosaic Agriculture of densely populated urban, commercial, industrial, residential, and agricultural matrices in Homestead, southeast Florida. Butterfly species richness, abundance and diversity were documented, providing valuable base-line data for on-going butterfly monitoring, and the importance of this site’s relatively healthy remnant ecosystems was evidenced by the supporting host plants for 20 migratory butterflies in 40 species. In addition, the air reserve base acts as refugia for many rare, endangered, and threatened federal and state-listed plants as well.

1. Introduction still common wildlife such as raccoons and opossums are squeezed into decreasing suitable habitat fragments within outheast Florida is a recognized ‘hotspot’ for urban matrices, the less-mobile, once-abundant species, [1] biodiversity , home to endemic rare plants and including small invertebrates, may become extirpated or Sanimals found nowhere else in the world, many extinct [4-12]. Remaining islands of natural ecosystems are of which are located in globally endangered ecosystems often infested with non-native, invasive plant and such as globally endangered pine rocklands [2] and tropi- species which exacerbate the ability of native wildlife to cal hardwood hammocks [3]. Even as human-tolerant and survive [5,7,9,11-17]. In addition, these fragments of remnant

*Corresponding Author: Sandy Koi, Conservation Associate, Entomology, Institute for Regional Conservation, 100 E. Linton Blvd., Suite 302B, Delray Beach, Florida, 33483, USA; Email: [email protected]; [email protected]

26 Distributed under creative commons license 4.0 DOI: https://doi.org/10.30564/jzr.v2i3.2063 Journal of Zoological Research | Volume 02 | Issue 03 | July 2020 habitat are usually surrounded by unsuitable, hostile envi- Service [41]: Bartram’s scrub-hairstreak (Strymon acis ronment with little safe connectivity between extant par- bartrami), Schaus swallowtail (Heraclides aristodemus cels [11,18-22]. The original pine rockland habitat, dominated ponceanus), Florida leafwing (Anaea troglodyta florida- by slash pines (Pinus elliottii var. densa) and rare endemic lis) and Miami blue (Cyclargus thomasi bethunebakeri) [42]. plants [23-26] has been reduced to less than 1.5% (Figure 1). Three additional species of butterflies in south Florida are Isolated safe haven areas (refugia) are often in danger of protected by the Florida Wildlife Conservation Commis- being lost to further commercial development, or agricul- sion [43] and 26 are considered “imperiled” in south Florida tural areas, affecting population size, survival and disper- by the State of Florida’s Imperiled Butterfly Work Group, sal capabilities [7,11,12,16,27-30]. a subset of the Florida Wildlife Conservation Commission [43], which was formed in 2008 to study declining lepi- doptera. Two species are now considered extinct, zestos ( zestos oberon) and Meske’s rockland grass skipper (Hesperia meskei pinocayo) [43]. Surveys of butterfly populations have been used as an important monitoring protocol for ecological and biodi- versity indicators for many years [12,39,44-48]. Our butterfly surveys show that the butterflies and plant species listed by the USFWS or FWC as endangered or threatened have safe refugia on the Homestead Air Reserve Base (HARB) (Figure 2); it is also valuable conservation data, strengthening long- term data collection that has been done in the Homestead area in nearby critical butterfly units[49] (Figure 3).

Figure 1. Remnant pine rockland areas remaining in Miami-Dade County are colored red; light gray outlines indicate original range Source: Fairchild Tropical Botanic Garden. Developed arenas invite increased use of pesticides and non-native vegetation, and vast agricultural monocultures not only use potentially harmful agrochemicals, insecti- cides and herbicides [15,31-35] but also heavy machinery that further degrades the soil structure and native vegetation (including removal of “weeds” that act as host plants for larvae and nectar sources for adult insects) [36]. In addition, South Florida agricultural lands consist of “rock- plowed” limestone outcrop, a process developed in the 1950’s to make use of the substrate called “Miami oolite” [37] for agriculture. Many butterfly species that inhabit this Figure 2. Homestead Air Reserve Base and surrounding unique environment are endemic to southeast Florida and matrices, located in southeast Florida [8,22,38-40] are often rare or localized . Four species are con- Source: Florida Natural Areas Inventory, 2002. Environmental Systems sidered endangered by the United States Fish and Wildlife Research Institute 2002.

Distributed under creative commons license 4.0 DOI: https://doi.org/10.30564/jzr.v2i3.2063 27 Journal of Zoological Research | Volume 02 | Issue 03 | July 2020

reducing the original base acreage by nearly half. Large portions were sold or transferred as excess property after Hurricane Andrew in 1992 [51]. The areas within the base are divided into fourteen “Land Management Units” [51] (Table 1); 1,000 acres are described as “heavily modified pine rockland habitat” [51]. The airfield itself covers 945.3 acres, nearly half of the remaining land area. Most of the units were either off-limits for surveys because of concern for safety, such as ordnance storage, or because of mili- tary practices, such as training sessions or other air force activities. Some ‘units’ actually consist of parking lots and administration buildings and were therefore not suitable for butterfly occupancy. There is a mosaic of non-native vegetation, native endangered or threatened plants, grass- lands, globally threatened pine rocklands, as well as old partially developed or damaged derelict areas. A lake and wetlands were not surveyed but are part of the off-limit areas to the southeast (runway area).

Table 1. Land management units identified on the base: (Integrated Natural Resources Management plan for Homestead Air Reserve Base, Homestead, Florida Volume Figure 3. Critical butterfly habitat units (in red) located 1, July 2009.) within proximity of Homestead Air Reserve Base Land Management Unit Acreage Source: M. Andrejko Boundary Canal 40,400 linear ft. Administrative and Industrial Support 334.3 acres 2. Location and Description of Survey Units Airfield Area 945.3 acres Grenade Range and Reserves Area 116.6 acres Homestead Air Reserve Base (HARB) is an active mil- Hush House Area 30.6 acres itary base located in southern Miami-Dade County, in Munitions Area 122.0 acres Homestead, Florida (25° 29’ 9.752”, -80° 23’ 27.298”). Northeast Grasslands 50.5 acres The base is located approximately 20 miles south-south- Operable Unit (OU)-2 acre 21.1 acres Phantom Lake (including old Grenade 93.8 acres west of the city of Miami and about 1.5 miles inland from Range) Biscayne National Park and the Atlantic Ocean (Figure 1). Remnant Pine Rockland 5.1 acres HARB is nestled within densely populated urban, com- SOCSouth 14.0 acres mercial, industrial, residential, and agricultural matrices. Southeast Triangle 51.9 acres The surrounding natural areas include globally endangered Southwest Clear Zone 57.0 acres pine rockland fragments, fresh-water marshes containing Twin Lakes and Wetland Fringe 40.8 acres Wetland marsh 34.7 acres low-lying herbaceous plants, coastal beaches with heavily used public and commercial boating facilities, tropical hardwood hammock fragments, mining operations, indus- 3. Descriptions of Survey Areas trial complexes and derelict abandoned properties (Fig- Pine Rockland Unit and Sample Site #7 ure 2). Agricultural fields are the predominant landscape On-going restoration at this northwest HARB pine rock- interspersed with residential, commercial and industrial land unit consisting of 5.1 acres was occurring as invasive facilities (such as limestone and sand mining). Critical non-native trees and exotic herbaceous vegetation were butterfly habitat units, protected natural areas owned and removed. The site contains mature and seedling Florida maintained by Miami-Dade County, or in some cases by slash pine trees (Pinus elliottii var. densa), a species par- private landowners, are located south, west, and north of ticular to south Miami-Dade and the Caribbean known for [40,50] the airbase (Figure 3). its extremely hard wood and high-leaved growth habit, HARB currently contains 1,943 acres; numerous own- due to being fire-adapted. The nutrient-poor limestone ership changes since the 1940’s and a number of powerful substrate in the rocklands has little soil or organic matter, hurricanes have caused significant damage over the years,

28 Distributed under creative commons license 4.0 DOI: https://doi.org/10.30564/jzr.v2i3.2063 Journal of Zoological Research | Volume 02 | Issue 03 | July 2020 and the pines grow slowly, making the wood dense and 3.1 Boundary Canal Unit hard. Other native trees in the pineland area included Flor- ida trema (Trema micranthum), the state-listed threatened The Boundary Canal unit consists of 40,400 linear feet (7.8 West Indian lilac (Miconia bicolor) and the state tree, cab- miles) of deep channels dug into the limestone substrate, bage palm (Sabal palmetto). Herbaceous plants include which contain fresh water with high visibility except for a the state-endangered pineland jacquemontia (Jacquemon- few areas polluted with urban trash that gets flushed into tia curtsii) and locustberry (Byrsonima lucida) (Figure 4). the canal from surrounding matrices. It harbors both na- tive and non-native fish, and occasional ducks and wading birds, as well as numerous non-native reptiles. Fresh-wa- ter canals such as these are known to provide habitat for the Miami cave crayfish, Procambus milleri,[52], a federally endangered species [43]. Weedy non-native tree seedlings and mature trees, pri- marily the exotic non-native Australian pine (Casuarina equisetifolia), line the edges of the canals. Native shrubs, such as myrsine (Myrsine floridana), and cocoplum (Chrysobalanus icaco), grow along the banks. Mainte- Figure 4. Remnant pine rockland area; this site has more nance protocol at the base periodically sprays herbicide understory vegetation than regularly fire-maintained pine along the canal edges, causing temporary die-back of all rockland areas (Copyright: Koi) vegetation. The Boundary Canal is shaded by the Austra- lian pine trees and non-native Brazilian pepper (Schinus Sample Site #7, a small subset of approximately 2 acres terebinthifolius) on the northwest and south routes and has located directly to the east of the pineland, consists of a grassy banks on the western route (Figure 6). few scattered mature and young Florida slash pines, and low-lying herbaceous native vegetation such as porterweed (Stachytarpheta jamaicensis), Spanish needle (Bidens alba var. radiata), and creeping ticktrefoil (Desmodium inca- num). The federally endangered sandflax, Linum( arenico- la), and the state-listed endangered quailberry (Crossopeta- lum ilicifolium) are also located here (Figure 5).

Figure 6. The southwestern edge of the boundary canal unit has a grassy bank with scattered trees along the canal, lined with non-native Australian pine and Brazilian-pep- per on the eastern edge (Copyright: Abbott)

3.2 Grenade Range and Reserves Unit

A grenade range and reserves area, still used for military practices, consists of 116.6 acres of open mowed and un- mowed grasslands, and thin sand-soils lying on limestone outcrop. There is a rich variety of both native and non-na- tive trees and vegetation. Native plants found include passionvine (Passiflora suberosa), porterweed, marlberry (Ardisia escallonioides), and sandflax (Linum areniola). There are sunny open areas of native and non-native Figure 5. Sample site 7 contains a ruderal field with grassy fields, both mowed and un-mowed. Native herbs scattered non-native Australian pine seedlings (now de- in this unit include passionvine, Spanish needles, pencil- stroyed) and native slash pine trees and seedlings. (Copy- flowers Stylosanthes( hamata) and native milkweed (As- right: Abbott)

Distributed under creative commons license 4.0 DOI: https://doi.org/10.30564/jzr.v2i3.2063 29 Journal of Zoological Research | Volume 02 | Issue 03 | July 2020 clepius suberosa), and the federally endangered Small’s pine rockland, and weedy un-mowed fields. It contains milkpea (Galactia smallii). There are also burned out twenty-six federal- and state-listed trees such as silver vehicles and other blockades from military practices on palm (Coccothrinax argentata), and Bahama senna (Senna this location, but we did not monitor near these artifacts. mexicana var. chapmanii). Some areas are densely over- Non-native Australian pine and Brazilian pepper trees are grown and heavily shaded with native plants such as the mixed among native trees such as gumbo limbo (Bursera semi-invasive jack-in-the-bush (Chromolaena odorata), simaruba), poisonwood (Metopium toxiferum) and willow an excellent nectar source for both butterflies and moths, bustic (Dipholis salicifolia) (Figures 7 and 8). as well as bees, beetles and other beneficial insects. Her- baceous vegetation such as the federally endangered sandflax, and Small’s milkpea are found here as is the state-listed endangered pineland clustervine (Jacquemon- tia curtsii). The area has a wide variety of small native shrubs, including beautyberry (Callicarpa americana), saltbush (Baccharis halimifolia), native trees such as wild tamarind (Lysiloma latisiliquum) and royal palm (Roysto- nea elata). Florida state-listed ground-covering herbs such as wild potato morning glory (Ipomoea microdactyla), Bahama ladderbrake (Pteris bahamensis) and pineland lantana (Lantana depressa). On-going non-native plant removal also occurred at this location, to remove heavy Figure 7. The practice Grenade Range and Reserves Area infestation of Brazilian pepper and Burma reed (Neyraudia consisted of mowed and unmown areas, as well as the der- reynaudiana) (Figure 9). elict vehicles used in military training sessions (Copyright: Koi)

Figure 9. Weedy un-mown fields surrounded by shrubs and slash pines dominate SOCSouth; scattered sections of old pavement are also located in this unit (Copyright: Koi)

4. Materials and Methods

Nine standard “Pollard Walk” [44] surveys were conduct- ed in four diverse ecosystems located on the base to Figure 8. The edge of the Boundary Canal northwest document butterfly species between 09-May-2015 and perimeter has a narrow grassy edge, shaded by a mix of 30-December-2016. Pollard walks are used throughout the non-native Australian pine and Brazilian-pepper trees; the world to assess butterfly populations, and primarily con- semi-shaded understory contained abundant weedy nec- sist of slowly walking along pre-determined set transects tar and host plant resources. A. Facing the canal looking or routes in the chosen site, noting butterfly species within west. B. Facing the trees looking east (Copyright: Koi) five meters on three sides (left, right and above). Care was taken to avoid double-counting as the insects flew and 3.3 Special Operations South (SOCSouth) close-focus binoculars were used to identify species; spe- cies were photographed whenever possible. Walks some- This 14-acre area consists of a mosaic of remnant derelict times had to be cancelled because of military exercises, road fragments, tropical hardwood hammock, restored

30 Distributed under creative commons license 4.0 DOI: https://doi.org/10.30564/jzr.v2i3.2063 Journal of Zoological Research | Volume 02 | Issue 03 | July 2020 heavy tropical storms, or restoration work, which accounts Florida trema (Trema mican- thrum) for the unevenness of the surveys. Martial scrub Strymon No Common Fanpetals (Sida hairstreak martialis Richness and diversity was determined using Shan- acuta); Elliott's Fanpetals (S. non-Weiner Diversity Index, and Simpson Dominance elliottii) Mallow scrub Strymon Sleepy Morning (Waltheria Index, as well as the Equitability Index, and skewness was No established via Kurtosis. Identification was done by an en- hairstreak istapa indica) Fulvous hair- Electrostry- Brazilian-pepper (Schinus tere- No tomologist (one of the authors, SK), aided when necessary streak mon angelia binthifolius) [53] with photographic records from a university website Common Fanpetals (Sida and a field guide[54] . acuta); Elliott's Fanpetals (S. elliottii) Strymon Gray hairstreak No Lead Tree (Leucaena leuco- melinus 5. Butterfly Survey Results cephala) Buttonwood (Conocarpus erec- Forty species of butterflies were counted, in seven fam- tus); polyphagous* ilies, for a total of 2,128 individuals in the nine Pollard Downy milkpea (Galactia volubilis); Small's Milkpea (G. Walks (Table 2). We recorded 469 individuals in the pine- Leptotes Cassius blue No smallii) land and Sample Site #7 (Figure 10), 1,425 individuals in cassius False Tamarind (Lysiloma latis- the Canal and Grenade Range (Figure 11), and 234 indi- iliquum) Sensitive Pea (Chamaecrista viduals in SOCSouth (Figure 12). (Boundary Canal and Hemiargus Ceraunus blue No nictitans var. aspera); Partridge Grenade Range were counted as one unit because they are ceraunus Pea (C. deeringiana) contiguous in the actual landscape.) Zebra heliconi- Heliconius Corkystem passionvine (Passi- No an charithonia flora suberosa) Julia heliconi- Corkystem passionvine (Passi- Table 2. Butterflies observed at Homestead Air Reserve Dryas iulia No Base by standard Pollard Walks from 9 May 2015 to 30 an flora suberosa) Agraulis Corkystem passionvine (Passi- Dec. 2016, migratory status and host plants on base Gulf fritillary Yes vanillae flora suberosa) Variegated Euptoieta Sand Flax (Linum arenicola ); Common Scientific Migra- Yes Hostplant(s) fritillary claudia Everglades Flax (L. carteri) Name Name tory Phyciodes Scaleleaf Aster (Symphyo- Pearl crescent No Wild Lime (Zanthoxylum faga- tharos trichum adnatum) Giant swallow- Papilio Yes ra); Other citrus in surrounding Turkey Tangle Fogfruit (Phyla tail cresphontes Phyciodes matrix Phaon crescent Yes nodiflora);Southern Fogfruit (P. phaon Peppergrass (Lepidium vir- stoechadifolia) ginicum); Other mustards in Buckeye, tropi- Junonia False Foxglove (Agalinis fascic- No Great southern Ascia mon- surrounding matrix cal genoveva ulata) Yes white uste Chapman’s Wild Sensitive Plant Buckeye, com- Junonia Sand Flax (Linum arenicola) Yes (Senna mexicana var. chap- mon coenia (?)** manii) Turkey Tangle Fogfruit (Phyla nodiflora);Southern Fogfruit (P. Pink-spot Aphrissa Wild tamarind (Lysiloma latisi- Anartia Yes White peacock Semi stoechadifolia) sulphur neleis liquum); Sabicu (L. sabicu) jatrophe Herb-of-Grace (Bacopa monn- Deering Partridge Pea (Cha- ieri) Cloudless Phoebis maecrista deeringiana); Ruddy dagger- Marpesia Strangler fig Ficus( aurea); Yes Yes sulphur sennae Sensitive Pea (C. nictitans var. wing petreus Laurel Fig (F. microcarpa) aspera) Danaus Scarlet Milkweed (Asclepias Monarch Yes Orange-barred Phoebis False Tamarind (Lysiloma latis- plexippus curassavica) Yes sulphur philea iliquum) Danaus Scarlet Milkweed (Asclepias Queen Semi gilippus curassavica) Beggarweed (Desmodium inca- Large orange Phoebis Beggarweed (Desmodium inca- Yes num); Threeflower Ticktrefoil Long-tailed Urbanus sulphur agarithe Yes num); Threeflower Ticktrefoil (D. triflorum) skipper proteus (D. triflorum); polyphagous* Chapman’s Wild Sensitive Plant Beggarweed (Desmodium inca- Little yellow Pyrisitia lisa Yes (Senna mexicana var. chap- Dorantes long- Urbanus Semi num); Threeflower Ticktrefoil manii) tail dorantes (D. triflorum); polyphagous* Partridge Pea (Chamaecrista Eurema Barred yellow Yes fasciculata); Deering Partridge Horace's Erynnis daira No Oak species (Quercus sp.) Pea (C. deeringiana) duskywing horatius Tropical Common Fanpetals (Sida Spanish Needles (Bidens alba Pyrgus checkered No acuta); Elliott's Fanpetals (S. Dainty sulphur Nathalis iole Yes var. radiata); Cheesytoes (Sty- oileus losanthes hamata) skipper elliottii) Neamathla Nastra nea- Bluestem grass (Andropogon No skipper mathla sp.)

Distributed under creative commons license 4.0 DOI: https://doi.org/10.30564/jzr.v2i3.2063 31 Journal of Zoological Research | Volume 02 | Issue 03 | July 2020

Three-spotted Cymaenes Guinea Grass (Panicum maxi- No skipper tripuncta mum) Clouded skip- Lerema Saint Augustine Grass (Steno- Yes per accius taphrum secundatum) Southern skip- Copaeodes Bermuda grass (Cynoden dac- No perling minimus tylon) Ancyloxypha Giant Cutgrass (Zizaniopsis Least skipper No numitor miliacea) Bermuda grass (Cynoden dac- Sachem skip- Atalopedes Yes tylon); Saint Augustine Grass per campestris (Stenotaphrum secundatum) Bermuda grass (Cynoden dac- Hylephila Fiery skipper Yes tylon); Saint Augustine Grass phyleus (Stenotaphrum secundatum) Baracoa skip- Polites bara- No Grass sp.; polyphagous* per coa Figure 12. SOCSouth butterfly distribution was dominat- Saint Augustine Grass (Steno- ed by butterflies in the Nymphalid family and had more Southern bro- Wallengre- No taphrum secundatum); Thin ken-dash nia otho Lycaenids than any other habitat on the base paspalum (Paspalum setaceum) The least represented species were swallowtails (Papil- Notes: *Polyphagous refers to a wide variety of food plants; most com- mon host plants are listed but these may not be the only host plants used ionid family), with only three individuals in one species, by the species. **Lineria is the usual hostplant; Linum may be as well the giant swallowtail (Papilio cresphontes), which was based on chemical composition comparisons[79-81]. also only seen in one count (Figure 13). There were seven species and 816 individuals of “whites and yellows” (Pier- id family) counted, the most abundant being barred yellow (Eurema daira), which accounted for 79% of the Pierids and 30% of all species. Dainty sulphurs (Nathalis iole) were the second most abundant in the family, accounting for 9% of all of the Pierids. Other species observed were great southern white (Ascia monuste), large orange sul- phur (Phoebis agarithe), little yellow (Eurema lisa), and orange-barred sulphur (Phoebis philea) (Figure 13).

Figure 10. Pine Rockland Unit and Sample Area #7 were dominated by Nymphalids and Pierids, with a few Lycae- nids and only one sighting of a Papilionid, which account- ed for less than 0.002% of the total individuals observed and is represented by 0% on the graph

Figure 13. All butterfly families and abundance docu- mented at Homestead Air Reserve Base counted by stan- dard Pollard Walks from 9 May 2015 to 30 Dec. 2016. The Papilionid count consisted of only three individuals, which was less than 0.001% of the total individuals ob- served, statistically counted as “0%” Figure 11. Species distribution in the practice Grenade The very small butterflies known as “blues” accounted Range and Boundary Canal Unit was dominated by the for 4% of all butterflies counted, in only two species, cer- Nymphalid and Pierid families aunus blue (Hemiargus ceraunus) and cassius blue (Lep-

32 Distributed under creative commons license 4.0 DOI: https://doi.org/10.30564/jzr.v2i3.2063 Journal of Zoological Research | Volume 02 | Issue 03 | July 2020 totes cassius). Although both species are common, both Skipper butterflies (Hesperidae family) were much less butterflies are listed as endangered by the federal govern- abundant than expected given the profusion and diversity ment [42], because of their similarity to the federally endan- of graminoid species in the grassy fields on the air base, gered Miami blue (Cyclargus thomasi bethunebakerii) [42]. as many skippers are grass feeders. Fourteen species were Ceraunus blue was more common than cassius blue (Figure observed, totaling 199 individuals. The most abundant 13). species was baracoa skipper (Polites Baracoa), represent- Only four species of “hairstreak” butterflies (Lycaenidae ing 31% of all skippers observed. Longtailed skippers family), named for the tiny tail-like protrusions on their (Urbanus proteus) were the next abundant, followed by hindwings, were seen. Numbering just 20 individuals, the Dorantes skipper (Urbanus dorantes). We also record- they accounted for less than 1% of the butterfly species ed fiery skipper (Hylephila phyleus), clouded skipper (Le- recorded. The most observed species was fulvous hair- rema accius), three-spotted skipper (Cymaenes tripunc- streak (Electrostrymon angelia). There was only one each tus), tropical checkered skipper (Pyrgus oileus), monk observed of mallow scrub-hairstreak (Strymon istapa), skipper (Asbolis capucinus), ocola skipper (Panoquina martial scrub-hairstreak (Strymon martialis), and gray ocola), sachem skipper (Atalopedes campestris), southern hairstreak (Strymon melinus) (Figure 13). broken-dash skipper (Wallengrenia otho), southern skip- The “Brushfoot” butterflies (Nymphalids) were the perling (Copaeodes minimus), least skipper (Ancyloxypha most abundant family observed at each survey, totaling numitor), neamathla skipper (Nastra neamathla), and pal- 933 individuals in nine species. Gulf fritillary (Agraulis metto skipper (Euphyes arpa) (Figure 13). vanillae) butterflies accounted for 46% of all Nymphalids Shannon Diversity Index shows fairly high diver- observed, and 34% of all butterflies observed, with 433 sity (2.554) dominated by a few species (Simpson’s individuals. White peacocks (Anartia jatrophae) were the Index of Dominance: 0.8612). The species evenness second most abundant. was low (0.692), and the skewness/Kurtosis was high We did not differentiate between the two possible (3.697/14.308). Southeast Florida buckeye butterflies tropical buckeye (Junonia zonalis) and common buckeye (J. coenia) (see 6. Discussion detailed note and citations regarding Junonia species Tracks of land protected from further development and and migration). Because buckeyes scatter quickly when alteration, such as HARB and other military and reserve approached, it was challenging to verify species consis- bases, act as vital refugia for plant and animal taxa, as tently in the field. The majority were likely “tropical” well as providing connectivity between remaining natural as opposed to “common” because the host plant for the areas, even in heavily urbanized surrounding matrices tropical buckeye, blue porterweed (Stachytarpheta jamai- [30,49,55] . However, the natural areas within these agricultur- censis), is abundant on the property. Tropical buckeyes do al-urbanized matrices may ‘suffer from detrimental edge not migrate, but common buckeye does. However, they [5-7,11,50,56] effects’ , primarily because the natural ‘edges’ hybridize in locations where they migratory route of the or ecotones no longer exist and the biotic taxa that may common buckeye overlaps with the resident populations have lived within the transition zone between ecosystems of the tropical species. For this reason, ‘buckeye’ species cannot adapt to the changes between a natural area and an were counted as one group. (The third species, mangrove artificial matrix. Butterflies and other insects often require buckeyes (J. evarete) are not found on the base as there specific elements in ‘landscape architecture’ as well as are no host plant mangroves on the surveyed property and host plants and nectar resources in order to persist in a lo- this species does not migrate. [20,57] cation . In addition, fire-maintained ecosystems such Zebra heliconian (Heliconius charithonia) was the next as pine rocklands suffer from fire suppression in urban abundant species seen, and we also observed variegated [50] areas . fritillary (Euptoieta claudia), phaon crescent (Phyciodes There was a pronounced difference in the abundance phaon), julia heliconian (Dryas iulia), pearl crescent (Phy- of butterflies in the different units (Table 3). The high- ciodes tharos) and ruddy daggerwing (Marpesia petreus) est number of species (34) and most individuals (1424) (Figure13). counted was in the Practice Grenade Range/Boundary Ca- There were 46 individuals counted in the milkweed nal Unit, which had the most habitat diversity and greatest butterfly family (Danaid), which are Nymphalids, 25 acreage. Weedy, overgrown, limestone outcrop areas such queens and 23 monarchs (Figure 13). No soldiers, the as the Pine Rockland and Sample Area 7 units hosted third Danaid species, were observed on base (pun intend- thirty species and we counted 469 individuals there. The ed)! lowest species count (29) and lower number of individuals

Distributed under creative commons license 4.0 DOI: https://doi.org/10.30564/jzr.v2i3.2063 33 Journal of Zoological Research | Volume 02 | Issue 03 | July 2020

(243) counted was in the SOCSouth Unit, which at that Three-spotted skip- Cymaenes 1 1 9 time was still undergoing restoration efforts. per tripunctus Clouded skipper Lerema accius 6 - 5 Copaeodes Table 3. Butterfly species abundance as observed in the Southern skipperling 1 - 1 units surveyed on Homestead Air Reserve Base minimus Ancyloxypha Least skipper 2 - 7 Pine Practice numitor Rock- Grenade Atalopedes SOC- Sachem skipper - 4 1 Common Name Scientific Name land/ Range/ campestris South Sample Boundary Hylephila Fiery skipper 8 1 4 Area 7 Canal phyleus Papilio cres- Giant swallowtail 1 - 2 Baracoa skipper Polites baracoa 32 3 30 phontes Southern bro- Wallengrenia 2 2 - Great southern white Ascia monuste 2 - 24 ken-dash otho Cloudless sulphur Phoebis sennae 8 7 29 Palmetto skipper Euphyes arpa 1 - - Orange-barred sul- Asbolis capuci- Phoebis philea 1 4 - Monk skipper 4 1 2 phur nus Phoebis Panoquina Large orange sulphur 1 4 7 Ocola skipper - 6 - agarithe ocola Little yellow Pyrisitia lisa 2 7 2 Total abundance 469 234 1424 Barred yellow Eurema daira 149 10 487 Total species 30 29 34 Dainty sulphur Nathalis iole 9 2 60 While many land managers must think in big pictures Martial scrub-hair- Strymon martia- - - 1 (saving biomes for bears or whales), the micro-scale at streak lis Mallow scrub-hair- which many insects live is something often overlooked: Strymon istapa 4 - 2 streak even small tracts of land, if providing necessary elements Electrostrymon Fulvous hairstreak - 13 - for survival, may be important for the persistence of rare angelia and endangered endemic taxa [17,19,20,22,30,49,56,57]. Fire-driv- Strymon meli- Gray hairstreak - 1 - nus en and fire-adapted pine rockland habitats may contain [37,58,59] Cassius blue Leptotes cassius 1 8 18 as many as 536 plant taxa and even small isolated Hemiargus fragments may contain exceeding rare or threatened spe- Ceraunus blue 25 11 39 ceraunus cies [38,59,60]. This is true for the HARB pine rockland unit, Heliconius Zebra heliconian 4 6 53 which contains four Florida state endangered plants, and charithonia Julia heliconian Dryas iulia 2 - 7 over fifty native plants. Only nine non-native plants were Agraulis vanil- found in the small pineland, which have since been eradi- Gulf fritillary 101 58 261 lae cated. Euptoieta clau- Variegated fritillary 11 18 3 The hostplants (larval food plants) for all butterfly spe- dia cies observed are found on the base, with the exception of Phyciodes thar- Pearl crescent - 3 1 os the recorded food for the palmetto skipper, saw palmetto Phyciodes pha- (Serenoa repens), (Table 2). It is possible that the palmetto Phaon crescent 3 1 29 on skipper is utilizing the other palm species located on the Buckeye species Junonia sp. 67 32 32 base, or saw palmetto located in nearby critical butterfly White peacock Anartia jatrophe 12 7 203 units (Figure 3). A wide variety of nectar sources is also Marpesia [59,60] Ruddy daggerwing - 2 1 site, providing continuous bloom appropriate for the petreus Danaus plexip- adults of all species (generally, small butterflies need Monarch 2 3 18 pus small flowers and large butterflies need large flowers). Queen Danaus gilippus 6 10 11 Homestead is also a “low-income” community (per capita [61] Urbanus prote- income is below $18K) , and there are many ‘less-man- Long-tailed skipper 1 6 48 us icured’ homes in the residential area, which is beneficial Urbanus dor- Dorantes longtail - 3 20 antes for weedy overgrowth of nectar and host plants in the Tropical check- surrounding matrix. Although the agricultural fields sur- Pyrgus oileus - - 6 ered-skipper rounding the base may provide some additional host and Nastra nea- Neamathla skipper - - 1 nectar sources, pesticide and herbicide use is also frequent mathla [6,35,50,62]. Florida has a year-round growing season.

34 Distributed under creative commons license 4.0 DOI: https://doi.org/10.30564/jzr.v2i3.2063 Journal of Zoological Research | Volume 02 | Issue 03 | July 2020

HARB is located on the eastern coast of south Florida, sites may act as “sinks” for some butterfly species, i.e., along the “Atlantic Flyway,” where birds, dragonflies the primary host plant may not be available, so a female and butterflies follow the trade winds to aid in migrating butterfly may choose inferior plants because that is all south or north, depending on season, increasing its value from which she has to choose at a remaining site [15,16,28-30,68]. as a stop-over site and refugia. One author (SK) witnessed In this scenario, the offspring may not survive, or may mass migrations of checkered whites (Pontia protodice) survive but not thrive, on the inferior or alternate host, and great southern whites flying through southern Home- causing the offspring to develop various inbred genetic stead, ovipositing and mating on the abundant peppergrass faults or weakened immune systems, and/or the surviving (Lepidium virginicum) growing along the edges of the adults may not be robust enough to mate and perpetuate agricultural fields, and then saw the farm workers come the colony [15,19,27,29,30,68,69] Because the butterflies are actu- out soon after to spray pesticide-herbicide to kill any and ally occupying a site is not always an indication that the all butterflies, eggs and larvae. Simply converting to agri- site is “high-quality habitat”; it may be all that is left for cultural fields from original habitats is destructive to most them [9,11,16,17,30,67,68]. butterfly assemblages, especially in tropical and neo-trop- For most butterfly species, we do not have the popula- ical regions[11,39,56]. The toxins from these anthropogenic tion viability analysis (PVA), which is how to determine chemicals are detrimental to development and survival if a colony is large enough to prevent collapse through of insect pest species in agricultural fields, but also affect genetic failure or food resource loss [30] and can calculate non-target butterflies and beneficial insects[6,31-35,39,62] . colony persistence for most . But what has been Of the 40 butterfly species observed, half (50%) are fairly well established is that habitat protection is of more long-distance migratory or at least exhibit a short distance importance and more telling for species survival that but wide dispersal [63,64] (Table 2). Besides the well-known PVAs, because butterflies do not have the same kind of monarchs, great southern and checkered whites, and gulf life history as mammals and avian species [30,40]. For exam- fritillaries (so named because they migrate across the Gulf ple, Longcore and Osbourne [30] point out that a “molehill” of Mexico), also migrate in swarms. Other butterflies mi- may indeed be a “mountain” for animals that are the size grate, but not long-distance, and some, such as the dainty of a dime or a quarter! Small urban preserves are increas- sulphur, may disperse as far north as New York. Barred ingly valuable for the survival of rare plants and insects yellow, dainty sulphur, great southern whites, gulf fritil- [16,17,30,40,49,66-68] and the risk of extinction increases with laries also exhibit periodic outbreaks or eruptions of large isolation from other sites [5,12,16,38,66] as well as connectivity numbers of individuals, often during migratory or disper- between habitat patches and the surrounding matrix of sal events [63,64]. those patches [6,16-18,66,70]. The giant swallowtails were seen in May, when the We were surprised that we did not see the federally en- citrus trees were in heavy flower and new foliar growth. dangered Bartram’s scrub-hairstreak, or Florida leafwing Three or more broods are known to occur in south Florida, butterflies on the base, as there are thousands of their and it is odd that we observed only these three swallow- sole host plant, pineland croton (Croton linearis) on the tails and no other swallowtail species. It may be that our surveyed sites. One author (SK) spoke to retired HARB surveys missed the main dispersal events for these butter- military personnel at a butterfly conference in 2015 who flies. mentioned that Bartram’s used to be present on the airbase The relative abundance of fulvous hairstreaks may during the 1950’s and 60’s. Possible reasons for extirpa- be attributed to the remaining regrowth of its only host tion of the butterflies include the increasing isolation of plant, the Brazilian pepper tree, one of the most aggres- this site from the other ‘critical butterfly units’ and pine sive non-native species on the base. The tree is ubiqui- rockland fragments in Homestead and south Miami-Dade tous throughout South Florida, even in areas that have County, because of increasing development of the sur- undergone restoration work. A Caribbean species, fulvous rounding matrix. In addition, HARB was heavily damaged hairstreak was first recorded in Florida in the early 1970’s, in Hurricane Andrew in 1992, and the presence of exotic arriving by unknown means; it is a rare example of a nat- animals and plants has exploded since then; there has uralized butterfly species that has benefitted from non-na- been inconsistent maintenance over the years because of tive plants. Invasive plants and animals have been asso- funding cuts and the absence of fire, as well as a number ciated with decreases in native species regardless of the of smaller but damaging hurricanes. ecosystems involved and non-native predators may also Not all butterfly species are able to adapt to living in ur- influence the survival of adults and offspring[8,10-17,50,65-67] . ban environments, although a few have managed to carve It is also noteworthy to remember that less-optimal out a niche in domestic gardens and botanical reserves;

Distributed under creative commons license 4.0 DOI: https://doi.org/10.30564/jzr.v2i3.2063 35 Journal of Zoological Research | Volume 02 | Issue 03 | July 2020 the atala butterfly (Eumaeus atala), a former denizen of All data and material are available via the Homestead Air the disappearing pine rocklands, has made itself quite at Reserve Base archives or the Institute for Regional Con- home in private gardens since the 1980’s with human as- servation with Department of Defense release. sisted re-location programs [17,21,66,67,70,71]. It is unlikely that either Bartram’s scrub-hairstreak or the Florida leafwing Code Availability will take to living in metropolitan backyards, but one can Not applicable. hope that such an event will take place should they be provided with sufficient host plant, landscape architecture, Authors’ Contributions and protection from urban pesticide use. In the meantime, HARB is acting as an important stop-over point and per- CVDH directed the study, SK designed and executed the manent refugia for butterflies and other migratory insects, surveys, CVDH and SK analyzed the data, SK wrote the such as dragonflies. manuscript and CVDH provided editorial advice.

Acknowledgments Ethics Approval

Michael J. Andrejko, GS-12 DAF Physical Scientist, is On behalf of, and having obtained permission from my thanked for on-going support and guidance; members co-author, I declare that: of the Broward County chapter of the North American (1) the material has not been published in whole or in Butterfly Society and biologist Cara Abbott (Institute for part elsewhere except as an original biological report to Regional Conservation) are thanked for survey help. We the Homestead Air Reserve Base, Homestead, Florida; thank both Jeffery M. Marcus and Marc C. Minno for dis- (2) the paper is not currently being considered for pub- cussion on the Junonia species. lication elsewhere; (3) both authors have been personally and actively in- Note on Junonia species volved in substantive work leading to the report, and will hold themselves jointly and individually responsible for We use the new species determination for the tropical its content; buckeye as Junonia zonalis, according to genetic analysis (4) all relevant ethical safeguards have been met in of the genus by Lalonde[72-74]. In the recent past, Turner [75] relation to patient or subject protection, or animal experi- and Parnell named the tropical buckeye as Junonia mentation. genoveva and the Mangrove Buckeye as Junonia evarete. There were no type specimens from the 1700’s, only col- Consent to Participate or illustrations in books published by Cramer[76]. Recent observations by Neild [77] reversed these names, but most Not applicable. scientists and older field guides stay with the descriptions Consent for Publication made by Turner and Parnell[75]. Lalonde’s seminal genet- ic work on the buckeye phylogeny is very valuable. It is Permission to publish was granted by Timothy F. Norton, known that the Junonia hybridize in South Florida and 482d Fighter Wing Public Affairs, Homestead Air Reserve possibly elsewhere, complicating identification[72-74,76,78] . Base, Homestead FL, on 11 Nov 2019. (786) 415-7330

Declarations References Funding [1] J.K. Myers, Norman, Mittermeier, Russell A., Mitter- meier, Cristina G., Gustavo A.B. da Fonseca. Nature, Funding was supported by a grant from the United States 2000, 403: 853-858. Department of Defense (FA6648-14-P-0023) to the Insti- [2] (n.d.). tute for Regional Conservation for surveys of butterflies [3] International Union for the Conservation of Nature and pollinators on Homestead Air Reserve Base, Home- and Natural Resources, 2016. stead, FL. [4] J. Tilden. News. 1956, 10: 133-145. [5] T.R. New, D.P.A. Sands. Journal of Insect Conserva- Conflicts of Interest tion. 2002, 6: 207-215. The authors proclaim there are no conflicts of interest. [6] K.-O. Bergman, J. Askling, O. Ekberg, H. Ignell, H. Wahlman, P. Milberg Bergman, K. Bergman karbe, O. Availability of Date and Material Ekberg, P. Milberg. Landscape Effects on Butterfly

36 Distributed under creative commons license 4.0 DOI: https://doi.org/10.30564/jzr.v2i3.2063 Journal of Zoological Research | Volume 02 | Issue 03 | July 2020

Assemblages in an Agricultural Region, n.d. [29] I. Saccheri, M. Kuussaari, M. Kankare, P. Vikman, W. [7] M.L. McKinney. Urban Ecosystems. 2008, 11: 161- Fortellus, I. Hanski. Nature. 1998, 392: 491-494. 176. [30] T. Longcore, K.H. Osborne, in: J.C. Daniels (Ed.). [8] M.C. Minno, American Butterflies. 2010: 16-22. Butterfly Conservation in North America, Springer [9] S. Fattorini. Biological Conservation. 2011, 144: Science + Business Media, 2010: 161-187. 370-375. [31] D. Pimentel. Journal of Agricultural and Environ- [10] D. Olle. American Butterflies. 2011: 4-14. mental Ethics. 1995, 8: 17-29. [11] M.F.J. Aronson, F.A. la Sorte, C.H. Nilon, M. Katti, [32] D. Pimentel. In: R. Peshin, A. Dhawan (Eds.). Inte- M.A. Goddard, C.A. Lepczyk, P.S. Warren, N.S.G. grated Pest Management: Innovation-Development Williams, S. Cilliers, B. Clarkson, C. Dobbs, R. Process. Springer Netherlands, 2009: 83-87. Dolan, M. Hedblom, S. Klotz, J.L. Kooijmans, I. [33] D. Pimentel, 2011. Kühn, I. Macgregor-Fors, M. Mcdonnell, U. Mört- [34] D. Pimentel, K. Hart, in: W. Galston, E. Shurr (Eds.). berg, P. Pyšek, S. Siebert, J. Sushinsky, P. Werner, M. New Dimensions in Bioethics: Science, Ethics and Winter, Proceedings of the Royal Society B: Biologi- the Formulation of Public Policy, Kluwer Academic cal Sciences, 2014, 281. Publishers, Boston. 2011: 79-108. [12] R. Dirzo, H.S. Young, M. Galetti, G. Ceballos, N.J.B. [35] T.C. Hoang, R.L. Pryor, G.M. Rand, R.A. Frakes. Isaac, B. Collen. Science. 2014, 345: 401-406. Environmental Toxicology and Chemistry, 2011, 30: [13] J. Ghazoul. Alien Abduction: Disruption of Native 997-1005. Plant-Pollinator Interactions by Invasive Species, [36] B. Badalíková. In: A.P. Dedousis, T. Bartzanas(Eds.), 2004. Soil Engineering, 2016. [14] R.K. Didham, J.M. Tylianakis, N.J. Gemmell, T.A. [37] J.R. Snyder, A. Hendron, W.B. Robertson., In: R.A. Rand, R.M. Ewers. Trends in Ecology and Evolution, Myers, J.J. Ewel(Eds.). Ecosytems of Florida. Uni- 2007. 22: 489-496. versity of Central Florida, 1990: 230-277. [15] D.L. Wagner, R.G. van Driesche. Annual Review of [38] T.R. New. Conservation Biology of Lycaenidae (But- Entomology. 2007, 55: 547-568. terflies), 1993. [16] D. Taron. In: Butterfly Conservation in North Ameri- [39] T.C. Bonebrake, L.C. Ponisio, C.L. Boggs, P.R. ca. 2015: 103-116. Ehrlich, Biological Conservation, 2010, 143: 1831- [17] L. Ramírez-Restrepo, S. Koi, I. MacGregor-Fors, Ur- 1841. ban Ecosystems, 2017, 20. [40] J. Diamond, J.T. Heinen. Urban Forestry and Urban [18] N.M. Haddad, K.A. Baum. Ecological Applications, Greening. 2016, 20: 1-11. 1999, 9: 623. [41] U.S. Fish and Wildlife Service, 2017. [19] P.B. Hardy, R.L.H. Dennis. The Impact of Urban De- [42] United States Fish Nd Wildlife Service (n.d.). velopment on Butterflies within a City Region, 1999. [43] Endangered and Threatened Species Management [20] M.D. Hunter. Agricultural and Forest Entomology. and Conservation Plan, n.d. 2002, 4: 159-166. [44] E. Pollard, D.O. Elias, M.J. Skelton, J.A. Thomas. [21] L. Ramírez Restrepo, G. Halffter. Landscape and Ur- Entomology Gazette, 1973, 26: 79-88. ban Planning. 2013, 115: 39-48. [45] C. Kremen. Wings. 1992, 16: 14-17. [22] L. Restrepo, I. MacGregor-Fors. Urban Ecosystems, [46] M. McGeoch. Biological Review. 1998, 73: 181-201. 2016. [47] P. Nowicki, J. Settele, P.Y. Henry, M. Woyciechows- [23] J.K. Small, Flora of Miami. Being Descriptions of ki. Israel Journal of Ecology and Evolution. 2008, the Seed-Plants Growing Naturally on the Everglade 54: 69-88. Keys and in the Adjacent Everglades, Southern Pen- [48] J. Gerlach, M. Samways, J. Pryke. Journal of Insect insular Florida, Small, J.K., 1913. Conservation. 2013, 17: 831-850. [24] J.K. Small. Journal of the New York Botanical Gar- [49] O. Cizek, P. Vrba, J. Benes, Z. Hrazsky, J. Koptik, dens. 1916: 37-45. T. Kucera, P. Marhoul, J. Zamecnik, M. Konvicka. [25] J.K. Small. From Eden to Sahara Florida’s Tragedy. PLoS ONE. 2013, 8. The Science Press Company, Lancaster, PA, 1929. [50] H.C. Giannini, J.T. Heinen. Natural Areas Journal. [26] J.K. Small, Flora of Miami, J.K. Small, 1913. 2014. [27] K. Zarzycki, J. Dabrowski. Acta Societatis Botani- [51] United States Department of the Air Force, Integrat- corum Poloniae, 1986, 55: 343-359. ed Natural Resources Management Plan for Home- [28] H.R. Pulliam, Sources, Sinks and Population Regula- stead Air Reserve Base, Homestead, Florida. Volume tionN, 1988. II. Appendices. Biological Resources. Appendix G,

Distributed under creative commons license 4.0 DOI: https://doi.org/10.30564/jzr.v2i3.2063 37 Journal of Zoological Research | Volume 02 | Issue 03 | July 2020

2009. [67] S. Koi, J. Daniels, Florida Entomologist, 2015, 98. [52] International Union for the Conservation of Nature [68] K. S. Entomology, Ornithology & Herpetology: Cur- and Natural Resources, 2016. rent Research, 2016, 06: 1-10. [53] K. Lotts, T. Naberhaus, 2017. [69] R. Frankham, K. Ralls. Nature. 1998. [54] J. Glassberg, M.C. Minno, J.V. Calhoun, Butterflies [70] E. Smith. A Field Study and Re-Establishment of the through Binoculars. A Field, Finding, and Gardening Butterfly Eumaeus Atala (Lycenidae) in Miami-Dade Guide to Butterflies in Florida. Oxford University County, Florida, 2000. Press, 2000. [71] S. Koi. Florida Entomologist, 2008, 91. [55] N.M. Haddad, K.A. Baum. An Experimental Test of [72] M.M.L. Lalonde, J.M. Marcus. The Journal of the Corridor Effects on Butterfly Densities, 1999. Lepidopterists’ Society, 2020. [56] B.W. Brook, N.S. Sodhl, P.K.L. Ng. Nature, 2003. [73] M.M.L. Lalonde, J.M. Marcus, Biological Invasions, [57] S. Brunzel, H. Elligsen, R. Frankl. Landscape Ecolo- 2019. gy, 2004. [74] M.M.L. Lalonde, B.S. McCullagh, J.M. Marcus. [58] K.A. Bradley. Assessment of Rare Plants and Pine Journal of the Lepidopterists’ Society, 2018. Rockland Habitat at Proposed US Army Special Op- [75] T. Turner, J. Parnell. Journal of Research on the Lep- erations Command South Headquarters Adjacent to idoptera, 1985. the US Air Reserve Base, Homestead Florida, 2009. [76] M.M.L. Lalonde. Biogeography and Genetic Popu- [59] C., C. Gann, GD. Stocking. Institute for Regional lation Structure of the Buckeye Butterflies (Genus Conservation (n.d.). Junonia) in the Western Hemisphere: Patterns of Hy- [60] G.D. Gann, K.A. Bradley, S.W. Woodmansee, 2001, bridization, Dispersal and Speciation, 2016. 2004. [77] A.F.E. Neild. The Butterflies of Venezuela. Part 2. [61] United States Census Bureau, 2010. Nymphalidae II (Acraeinae, Libytheinae, Nymph- [62] T.A. Bargar., Environmental Toxicology and Chem- alinae, Ithomiinae, Morphinae). A Comprehensive istry, 2012. Guide to the Identification of Adult Nymphalidae, [63] T.J. Walker. Ecological Entomology, 1991, 16: 241- Papilionidae, and Pieridae., Meridian Publications, 252. London, 2008. [64] R. Cech, G. Tudor. Butterflies of the East Coast. An [78] A.P. Gemmell, T.E. Borchers, J.M. Marcus. Psyche Observer’s Guide, Princeton University Press, 2005. (London), 2014. [65] Eds. Langeland K.A., Burks K.C. Identification and [79] Sigma-Aldrich, 2010. Biology of Non-Native Plants in Florida’s Natural [80] T. Cheriet, I. Mancini, R. Seghiri, F. Benayache, S. Areas Inventory Areas., University of Florida, IFAS, Benayache. Natural Product Research, 2015. Gainesville, FL, Gainesville, Florida, 1998. [81] K. Mizuochi, T. Tanaka, I. Kouno, T. Fujioka, Y. [66] S. Koi. Ecology and Conservation of Eumaeus Atala Yoshimura, K. Ishimaru. Journal of Natural Medi- Poey 1832 (Lepidoptera: Lycaenidae), 2013. cines, 2011.

38 Distributed under creative commons license 4.0 DOI: https://doi.org/10.30564/jzr.v2i3.2063