Caribbean Naturalist

No. 52

Caribbean Naturalist

2018

Abundance and Distribution of Brevipalpus (Acari: Tenuipalpidae) in the Residential Rio Piedras Watershed of San Juan’s Metropolitan Area of Puerto Rico

Amanda L. Henderson, Elvia J. Meléndez-Ackerman, and José Carlos V. Rodrigues

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Cover Photograph: Brevipalpus mite colony reared on citrus fruit arena in the Center for Excellence in Quarantine and Invasive Species, San Juan, PR.. Photograph © Jose Carlos and Amanda Henderson.

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CARIBBEAN NATURALIST

James D. Ackerman, Department of Biology, University of Puerto Rico at Río Piedras, USA Alfonso Aguilar-Perera, Department of Marine Biology, Universidad Autónoma de Yucatán, Mexico Wayne J. Arendt, International Institute of Tropical Forestry, Luquillo, Puerto Rico, USA Rüdiger Bieler, Field Museum of Natural History, Chicago, IL, USA Christopher P. Bloch, Department of Biological Sciences, Bridgewater State University, Bridgewater, MA, USA William R. Buck, Institute of Systematic Botany, New York Botanical Garden, Bronx, NY, USA Leo Douglas, Department of Geography/Geology, University of the West Indies, Mona, Jamaica Robert Erdman, Department of Biological Sciences, Florida Gulf Coast University, Fort Myers, FL, USA Keith Goldfarb, GoldRush Science Services, Steuben, ME, USA ... Editor-in-Chief Grizelle González, International Institute of Tropical Forestry, San Juan, Puerto Rico, USA Gary R. Graves, Department of Vertebrate Zoology, Smithsonian Institution, Washington, DC, USA Scott Jones, Smithsonian Institution, Caribbean Coral Reef Ecosystems, Carrie Bow Cay, Belize Heather Judkins, Department of Biological Sciences, University of South Florida, St. Petersburg, FL, USA John Leavengood, USDA-APHIS-PPQ, Tampa Bay, FL Joerg-Henner Lotze, Eagle Hill Institute, Steuben, ME, USA ... Publisher Antonio A. Mignucci-Giannoni, Manatee Conservation Center, Inter American University, Bayamón, Puerto Rico, USA Gregg Moore, Department of Biological Sciences, Jackson Estuarine Laboratory, University of New Hampshire, Durham, NH, USA Dawn Phillip, Department of Life Sciences, University of The West Indies, St. Augustine, Trinidad and Tobago... Managing Editor Robert Powell, Department of Biological Sciences, Avila University, Kansas City, MO, USA Chris Rimmer, Vermont Center for Ecostudies, Norwich, VT, USA Noris Salazar Allen, Smithsonian Tropical Research Institute, Panama Amy Siuda, Collegium of Natural Sciences, Eckerd College, St. Petersburg, FL, USA J. Angel Soto-Centeno, Rutgers University, Department of Biological Sciences, Newark, NJ, USA David W. Steadman, Florida Museum of Natural History, Gainesville, FL, USA Kathleen Sullivan Sealey, Department of Biology, University of Miami, Coral Gables, FL, USA Jarrod M. Thaxton, Department of Biology, University of Puerto at Mayagüez, USA Jason M. Townsend, Hamilton College, Biology Department, Clinton, NY, USA Jill Weber, Eagle Hill Institute, Steuben, ME, USA ... Production Editor Byron Wilson, Department of Life Sciences, University of the West Indies at Mona, Kingston, Jamaica Graham A. J. Worthy, Department of Biology, University of Central Florida, Orlando, FL, USA Joseph M. Wunderle, International Institute of Tropical Forestry, University of Puerto Rico at Río Píedras, USA

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2018 2018

Caribbean Naturalist CARIBBEAN NATURALIST A.L. Henderson, E.J. Meléndez-Ackerman, and J.C.V. Rodrigues

No. 52 No. 52:1–12

Abundance and Distribution of Brevipalpus (Acari: Tenuipalpidae) in the Residential Rio Piedras Watershed of San Juan’s Metropolitan Area of Puerto Rico Amanda L. Henderson1,*, Elvia J. Meléndez-Ackerman2, and José Carlos V. Rodrigues3 Abstract - Numerous studies have highlighted the significance of the mite genus Brevipalpus (Acari: Tenuipalpidae), which has risen from virtual obscurity to that of economic importance over the last few decades. There are 3 Brevipalpus mite species known to colonize a substantial number of fruit crops and infect them with deadly viruses; it has been shown that ornamental plant species can also serve as hosts to Brevipalpus. The high volume of trade and frequent movement of live ornamental plants make Brevipalpus pests of concern in terms of its dispersal potential. We conducted this study in the San Juan metropolitan area of Puerto Rico, where prior biodiversity studies indicated an overabundance of introduced ornamental shrubs. For this survey, we encountered a total of 62 plant species, out of which 23 (37%) acted as hosts plants to 548 individual Brevipalpus mites. These plant species were distributed across 16 families, with a total of 16 plant species not previously reported as Brevipalpus host plants. The native-to-exotic stem ratio differed significantly across the 4 sites surveyed in terms of frequency of those hosting Brevipalpus mites (χ2 = 7.64, P = 0.05, df = 3).

Introduction Mites (Subclass Acari) are the most diverse group of arthropods (Walter and Proctor 2013) and the most heterogeneous cheliceran group in terms of their morphological, biological, and ethnological diversity and their ability to colonize different environments (Vásquez et al. 2012). As a diverse lineage, mites often fill many niches and take on different functional roles within ecological communities. Phytophagous mites, which includes some Prostigmatan mites—chiefly spider mites, flat mites or false spider-mites, and eriophyid mites—use their specialized mouthparts to feed on the vascular tissues of plants (Bobot et al. 2011, Childers and Rodrigues 2011, Kondo et al. 2003). These mites are economically important pests because their activity can cause losses to field and greenhouse crops (Vásquez et al. 2012). Prostigmata mites have a considerable number of hosts, including fruits, ornamental and forest plants, and humans (Miranda et al. 2007). Childers et al. (2003) reported the phytophagous mite Brevipalpus (Tenuipalpidae) has 928 hosts in 513 Department of Biological Sciences, University of Illinois at Chicago, 845 West Taylor, Chicago IL 60607, USA. 2College of Natural Science, Department of Environmental Sciences, University of Puerto Rico-Rio Piedras, San Juan, PR 00936 ,USA. 3Center for Excellence in Quarantine and Invasive Species, Agricultural Experimental Station-Rio Piedras, Agro-Environmental Sciences Department, University of Puerto Rico-Mayaguez, 1193 Calle Guayacán, San Juan, PR 00926, USA. *Corresponding author - [email protected]. 1

Manuscript Editor: Ron Ochoa 1

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genera and 139 families. These mites, commonly referred to as flat mites or false spider-mites, comprise a complex group of species that are often redescribed into species types (Beard et al. 2015, Návia et al. 2013). Brevipalpus mites usually feed on lower leaf-surfaces, aggregating along the mid-vein or major lateral veins where they inject toxic saliva into fruits, leaves, stems, and bud tissues of their host plant (Vásquez et al. 2012). Numerous studies have highlighted the significance of the genus Brevipalpus (Childers and Derrick 2003, Miranda et al. 2007, Rodrigues and Childers 2012). They are a major threat to agricultural plants not because of their phytophagous nature but because they are known vectors of virus-borne plant diseases collectively referred to as leprosis. The most important Brevipalpus-associated viruses are the Citrus Leprosis virus (Rodrigues et al. 2003), Coffee Ringspot virus (Chagas et al. 2003), Passion Fruit Green Spot virus (Kitajima et al. 2003), Ligustrum Ringspot virus (Rodrigues and Nogueira 1996), and the Orchid Fleck virus (Bobot et al. 2011, Childers and Rodrigues 2011, Kondo et al. 2003). Leprosis is a widespread disease on Citrus spp. in most of South America, Central America, and a few parts of Southern Mexico (Rodrigues and Childers 2012). It can cause severe damage on trees, reduce yield, and even result in tree death if measures are not immediately taken to control mite populations (Rodrigues 2000). Brevipalpus is widespread, and viruses associated with that genus of mites have been observed in the tropics as well as in Australia, Denmark, Germany, Japan, Korea, and the US (Kondo et al. 2006). The globalized distribution of Brevipalpus may be a byproduct of the ornamental-plant trade (Miranda et al. 2007). Ornamental plants are a dominant fixture of urban green spaces (Vila-Ruiz et al. 2014), which may, as a result, serve as repositories of introduced pests including Brevipalpus mites (Miranda et al. 2007). Whether these organisms are uniformly widespread at a local scale or instead respond to differences in vegetation composition is not well known. The island of Puerto Rico has an active trade of fresh agricultural commodities, which has been on the increase since 1987 (Alamo et al. 2004). The introduction of exotic pests as a result is an ongoing phenomenon on the island and a major concern from an environmental management and economic perspective (Alamo et al. 2004). Residential yards are one of the most abundant land-uses within the San Juan metropolitan area (Ramos-González 2014). Introduced ornamental shrubs are the most common vegetation, but their diversity and abundance vary considerably throughout the city (Vila-Ruiz et al. 2014). Thus, the presence of Brevipalpus in residential yards is likely widespread. Our study sought to determine whether the abundance of Brevipalpus is related to the plant-community composition, plant complexity (diversity), and abundance in residential yards in the San Juan metropolitan area. We surveyed ornamental shrubs across residential areas of the San Juan metropolitan area to verify the presence of Brevipalpus and their hosts. We tested various hypotheses about the potential associations between the diversity and abundance of Brevipalpus mite communities and the vegetation abundance and composition of residential yards within the Rio Piedras watershed in the San Juan metropolitan area. In doing so, we considered the interaction between Brevipalpus and ornamental plants as a regular herbivore–plant 2

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interaction, where the dynamics of Brevipalpus could be regulated by bottomup (plant resource availability) or top-down controls (predators or competitors) (Shurin 2012). Knowing that plant communities vary somewhat predictably in their diversity, structure, and composition across habitats and biogeographic zones (Gurevitch et al. 2002); it is practical to hypothesize that the abundance and diversity of Brevipalpus may also vary predictably in relation to plant composition and diversity (Agrawal et al. 2006). For this study, we assumed that if Brevipalpus mite communities had a bottomup regulation, then their diversity and abundance would show a positive association with plant density and diversity. We expected plant communities that are less complex (low diversity) to yield simpler Brevipalpus communities (lower abundance) relative to ones that are more complex. Field-site Description We carried out our study in 4 urban residential areas within the Rio Piedras watershed (RPWS) in the San Juan metropolitan area, which includes the municipalities of San Juan, Trujillo Alto, and Guaynabo. RPWS is an urban watershed that covers an area of 49 km2 and has a mean annual rainfall that varies from 1509 mm on the coast to 1755 mm in the uplands (~8 km inland) and a mean annual temperature of 25.7 °C (Lugo et al. 2011). Natural areas within the watershed consist of a conglomerate of vegetation formations including forests, pastures, freshwater herbaceous wetlands, riparian vegetation, and ephemeral and/or dispersed vegetation that emerges in abandoned lots throughout the city (Lugo et al. 2011). However, in some areas of the watershed, private residential yards account for most of the available green space (Ramos-González 2014). Residential yards within the RPWS support over 400 species of plants (68% introduced species); shrubs are numerically dominant (Vila-Ruiz et al. 2014). Methods Vegetation measurements We carried out surveys of yard vegetation in June 2013 in 4 fixed locations within the RPWS (Puerto Nuevo, San Patricio, Avenida Central, La Sierra; Fig. 1) that had previously been surveyed for yard biodiversity. We randomly selected 5 houses within each residential area and noted the ornamental species, trees, and shrubs in the front yard of each, taking photographs of leaves, stems, flowers, and fruits when present to facilitate species identification. We determined if any of the plant species we documented was a reported host species of Brevipalpus based on prior literature reports (Childers et al. 2003, Kitajima et al. 2010, Miranda et al. 2007). For each house surveyed, we recorded its GPS location as well as the following variables: front-yard area, number of plant species per yard, the number of stems per yard (abundance) and leaf-sample biomass (see below for collection methodology) for each plant species collected, and the proportion of plant species with Brevipalpus mites. We used those variables to estimate plant density (number 3


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of stems/yard area) and the Shannon’s species-diversity index for the vegetation, calculated as: S

H' = - Σ pi * lnpi i=1

where S is the total number of species in the community (richness), pi is the proportion of S made up of the ith species. We also analyzed native:exotic plant-stem ratio, leaf biomass, and mite density (number of Brevipalpus/unit dry biomass). Brevipalpus extraction and sorting We followed a modified protocol by Miranda et al. (2007 to conduct mite fieldsampling and screening for Brevipalpus. For each plant species identified, we collected mature leaves from the inside of the canopy. Leaf samples varied from 1 to 20 leaves depending on the size and availability of plant material. We immediately washed and vigorously agitated the leaves in a bucket containing 200 mL of 80% ethanol. We saved the ethanol wash labeled with the plant-identification number. The leaves were then rinsed in water, placed in paper bags (also labeled with the plant-identification number and location record), dried at 60 °C for 48 h, and weighed to determine dry weight. In the laboratory, we poured each ethanol wash into a Petri dish divided into multiple 1-cm2 grids and examined the contents under a stereomicroscope (10–50x magnification) for the presence of Brevipalpus mites. We counted all Brevipalpus mites detected, which were then saved and stored in high-concentration ethanol. We slide-mounted 1–10 mites in Hoyer's mounting medium and oven-cured them

Figure 1. Sampling sites within the Rio Piedras watershed in the San Juan metropolitan area of Puerto Rico. Color image constructed in Google Earth Pro V 7.1.8.3036. 4

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at 43–45 °C for 2 weeks for identification (Krantz 2009). We deposited all mounted specimens in Dr. José Carlos Verle Rodrigues’s lab at the University of Puerto RicoMayagüez Experimental Station at the Botanical Garden in San Juan. Data analyses We employed Kruskal-Wallis tests to examine differences in the abundance of Brevipalpus mites across sites, the proportion of plant species infested with Brevipalpus mites, plant density, species diversity, and the ratio of native to nonnative species. We tested associations between mite density and the proportion of infested plants/yard with plant density, species diversity, and the ratio of native to non-native species in yards by comparing the mean values for each variable per site (n = 4). We performed all analyses in JMP version 4.0. Results Plant composition We recorded a total of 62 ornamental plant species (Table 1), of which over half (67.7%) were observed at only 1 house, 24.2% at 2 houses, and the remaining 8% at ≥3 houses. The 4 most common ornamental plant species surveyed were Ixora coccinea L. (Scarlet Jungleflame) found at 9 houses, Codiaeum variegatum (L.) Rumph. ex A. Juss (Garden Croton) found at 7 houses, Schefflera arboricola (Hayata) Merr. (Dwarf Umbrella Tree) found at 6 houses, and Dracaena marginata Lam. (Dragontree) found at 6 houses, all of which are non-native to the island of Puerto Rico. Most plants recorded in this survey were non-native plants (Table 1). Brevipalpus host plants Out of 20 yards surveyed, 70% hosted Brevipalpus on the surface of plant leaves, and nearly 83% of the mite occurrences were on non-native plant species. Twenty-three (37%) plant species acted as hosts plants to 548 Brevipalpus mites (Table 1). These plant species were distributed across 16 families and 21 genera. Sixteen plant species recorded had not been previously reported as Brevipalpus host plants (Table 1). We documented the Xanthorrhoeaceae and Linderniaceae as 2 new host families, hosting 21 and 9 Brevipalpus individuals, respectively. The most abundant plant hosts were Solenostemon scutellarioides (L.) Codd (Coleus) and Acalypha wilkesiana Müll. Arg. (Copperleaf), which hosted 186 and 146 Brevipalpus mites, respectively. All native plants (11 species) hosted Brevipalpus mites. We documented an average of 24 individuals per host plant regardless of plant origin. The mean abundance of Brevipalpus mites was not significantly different among sites by plant density (χ2 = 2.63, P = 0.45, df = 3), plant-species diversity (χ2 = 0.64, P = 0.88, df = 3), leaf biomass (χ2 = 2.09, P = 0.55, df = 3), or the proportion of plants hosting Brevipalpus (χ2 = 6.00, P = 0.11, df = 3). However, the native:exotic stem ratio did differ significantly in Brevipalpus abundance by site (χ2 = 7.64, P = 0.05, df = 3). There were no significant differences across sites in frequency of yards hosting Brevipalpus mites nor in the abundance of Brevipalpus per biomass of 5

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Table 1. Evaluation of yard-plant species for the presence or absence of Brevipalpus mites and their reported host status in the literature (Y = yes, N = no). A total of 548 Brevipalpus mites were observed in 16 families, with 16 new host species. AHost family. BNewly documented plant host, CGenus previously listed as host without including species name. [Table continued on following page.] Family/species name Origin

Yards w/ Host # of species sp. Brev.

AcanthaceaeA Crossandra infundibuliformis (L.). Nees Non-native 2 YB 9 Graptophyllum pictum (L.) Griff. Non-native 1 N 0 6 Ruellia caerulea Morong Non-native 1 YC A Agavaceae Cordyline fruticosa (L.) A. Chev. Non-native 1 YC 12 Nolina recurvata (Lem.) Hemsl. Non-native 1 N 0 AnnonaceaeA Annona muricata L. Non-native 1 Y 0 ApocynaceaeA Tabernaemontana divaricata (L.) R.Br. ex Roem. & Schult. Non-native 2 YC 1 AraceaeA Anthurium crenatum (L.) Kunth Native 1 YC 1 Dieffenbachia seguine (Jacq.) Schott Non-native 2 N 0 Monstera deliciosa Liebm. Non-native 1 Y 0 Philodendron sp. Non-native 1 Y 0 Spathiphyllum wallisii Regel Non-native 1 YB 2 Syngonium podophyllum Schott Non-native 1 YB 3 A Araliaceae Schefflera arboricola (Hayata) Merr. Non-native 6 Y 9 ArecaceaeA Dypsis lutescens (H.Wendl.) Beentje & J.Dransf. Non-native 4 N 0 AsparagaceaeA Dracaena marginata Lam. Non-native 6 N 0 Yucca gloriosa L. Non-native 1 N 0 BegoniaceaeA Begonia nelumbiifolia Cham. & Schltdl. Non-native 1 N 0 BignoniaceaeA Tecoma stans (L.) Juss. ex Kunth Non-native 1 Y 1 Bromeliaceae Bromeliaceae sp. Non-native 2 N 0 CombretaceaeA Conocarpus erectus L. Non-native 1 Y 0 CupressaceaeA Cupressus sempervirens L. Non-native 1 Y 0 EuphorbiaceaeA Acalypha wilkesiana Müll. Arg. Non-native 1 Y 146 Codiaeum variegatum - narrow (L.) Rumph. ex A. Juss Non-native 4 Y 5 Codiaeum variegatum - broad (L.) Rumph. ex A. Juss Non-native 3 Y 0 Euphorbia milii Des Moul. Non-native 1 NC 0 Euphorbia leucocephala Lotsy Non-native 1 NC 0 Jatropha curcas L. Non-native 1 Y 0 Fabaceae Pterocarpus indicus Willd. Non-native 1 N 0 LamiaceaeA Clerodendrum paniculatum Moldenke Non-native 2 Y 16 Clerodendrum quadriloculare (Blanco) Merr. Non-native 1 YC 25 Solenostemon scutellarioides (L.) Codd Native 2 YC 186 6

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Table 1, continued. Family/species name Origin

Yards w/ Host # of species sp. Brev.

Leeaceae Leea coccinea Planch. Non-native 2 N 0 LinderniaceaeA, B Torenia sp. Non-native 1 YB 9 LythraceaeA Lagerstroemia indica L. Non-native 1 NC 0 Lagerstroemia speciosa (L.) Pers. Non-native 1 YC 2 MalvaceaeA Hibiscus rosa-sinensis L. Non-native 1 Y 0 Thespesia grandiflora DC. Native 1 YC 28 MoraceaeA Ficus benjamina L. Non-native 1 YC 0 A Musaceae Heliconia sp. Non-native 1 Y 0 Heliconia psittacorum L.f Non-native 1 YC 1 Heliconia psittacorum L.f Non-native 2 NC 0 Musa paradisiaca L. Non-native 1 Y 0 NyctaginaceaeA Bougainvillea glabra Choisy Non-native 2 Y 0 Bougainvillea spectabilis Willd. Non-native 1 N 0 OleaceaeA Jasminum multiflorum (Burm. f.) Andrews Non-native 2 Y 0 Jasminum sambac (L.) Aiton Non-native 1 Y 0 OrchidaceaeA Spathoglottis plicata Blume Non-native 2 N 0 PassifloraceaeA Turnera ulmifolia L. Non-native 1 N 0 PlumbaginaceaeA Plumbago auriculata Lam. Non-native 1 Y 0 RosaceaeA Rosa indica L. Non-native 2 Y 0 RubiaceaeA Gardenia jasminoides J. Ellis Non-native 1 Y 0 Ixora coccinea L. Non-native 9 Y 0 Mussaenda frondosa L. Non-native 1 YC 1 Ruscaceae Dracaena sanderiana Mast. Non-native 1 N 0 RutaceaeA Citrus aurantifolia (Christm.) Swingle Non-native 1 Y 0 Murraya paniculata (L.) Jack Non-native 1 Y 0 SolanaceaeA Brunfelsia pauciflora (Cham. & Schltdl.) Benth. Non-native 1 Y 0 Cestrum diurnum L. Native 2 Y 25 XanthorrhoeaceaeA, B Dianella tasmanica 'variegata' Hook.f. Non-native 2 YB 21 A Zamiaceae Zamia furfuracea L.f. Non-native 1 N 0 ZingiberaceaeA Alpinia purpurata (Vieill.) K. Schum. Non-native 2 Y 38 Alpinia zerumbet (Pers.) B.L. Burtt & R.M. Sm. Non-native 1 YC 1 7

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vegetation (Table 2). Likewise, there were no significant differences in plant abundance or diversity across sites, but for this study, the yards sampled in Puerto Nuevo tended to have more native species than those of houses at other sites (Table 2). Discussion Our combined vegetation results suggest that the occurrence of Brevipalpus mites in urban yards of the RPWS is likely to be widespread, given that Brevipalpus was present at 70% of the house sites surveyed and 37% of the plant species recorded (Table 1). In addition, while over a third of the plant species surveyed were hosts, those 62 species represent a small fraction of the total number of plants that are present in residential yards at these 4 sites (~400 species; Villa-Ruiz et al. 2014). A rigorous, expanded study encompassing the entire Rio Piedras area is needed to determine the extent of Brevipalpus’ local distribution and presence on other ornamental species. Brevipalpus has been described as a generalized plant herbivore (Vásquez et al. 2012). The diversity of plant families and plant genera that are represented across the host species identified in this study would seem to support the suggestion of Brevipalpus as a generalist. Our study detected a large number of ornamental plants previously undocumented as hosts, thus indicating that there is a gap of information in relation to the host range of this group of mites (Childers et al. 2003, Kitajima et al. 2010, Miranda et al. 2007, Návia et al. 2013). Consistent with findings in other tropical sites, most of the infested plant species were non-native ornamentals (Childers et al. 2003, Kitajima et al. 2010, Miranda et al. 2007). Although all native plants were infested with Brevipalpus, the 2 species with the highest density of mites, Copperleaf and Coleus, are non-native. Coleus is frequently susceptible to larger arthropod pests like Planococcus citri (Risso) (Citrus Mealybug; Hogendorp et al. 2006, Lim et al. 2011) and has been shown to be a frequent host plant (Chong et al. 2005). While Copperleaf is known to have chemical defensive properties against bacteria and fungi (Alade and Irobi 1993), this plant species is a known host for multiple economically devastating species of Brevipalpus mite (Miranda et al. Table 2. Kruskal-Wallis analyses testing for differences across sites (CA = Avenida Central, LS = La Sierra, PN = Puerto Nuevo, SP = San Patricio) in vegetation and Brevipalpus characteristics. Values for sites are given as mean ± SE.

Site

Plant density (number of plants/m2)

CA LS PN SP

0.71 ± 0.22 0.30 ± 0.08 0.62 ± 0.25 0.40 ± 0.07

1.23 ± 0.11 1.32 ± 0.11 1.20 ± 0.21 1.10 ± 0.24

χ2 P

2.63 0.45

0.64 0.88

*

Plant Native:exotic diversity (H') stem ratio 0.08 ± 0.05 0.12 ± 0.07 0.52 ± 0.15 0.15 ± 0.06

Number of Brevipalpus/ leaf biomass (g)

Proportion of plants with Brevipalpus

0.43 ± 0.55 0.93 ± 0.88 0.14 ± 0.09 0.22 ± 0.11

0.42 ± 0.10 0.27 ± 0.08 0.08 ± 0.05 0.18 ± 0.11

7.64 2.09 6.00 0.05* 0.55 0.11

Significant at P = 0.05. 8

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2007), and our observations of the dense infestation of Copperleaf by Brevipalpus suggest that these mites can successfully combat those defenses. Except for native:exotic stem ratio, the lack of association between Brevipalpus abundance and traits related to yard vegetation might be an artifact of the low degree of front-yard variation in these highly urbanized sites or the small sample size. Future studies involving larger sample sizes might clarify some of the non-significant trends we observed. For example, we found a tendency for Brevipalpus to be less common in yards with higher species diversity. Also, the 4 sample locations varied noticeably in the proportion of plants that carried Brevipalpus species even when they were similar in levels of plant diversity (Table 1), but this trend was also not statistically significant. These large variations in the frequency of yards occupied by Brevipalpus could potentially be attributed to differences in any number of unmeasured abiotic factors (i.e., percent relative air humidity, temperature) across sites. To illustrate, the Puerto Nuevo residential area, with only 2 house sites out of 5 with Brevipalpus, has yards with high percentages of impervious groundcover (Meléndez-Ackerman et al. 2016), where yards may be hotter and less humid than those at the other sites. These conditions may not be as suitable for Brevipalpus colonization, as suggested by findings that mites are generally found in more shaded areas on host plants in more-humid environments, thus avoiding higher temperature conditions on sun-exposed plant surfaces (Childers and Rodrigues 2011). These unmeasured factors should be considered in future studies that evaluate optimal conditions for Brevipalpus and identify distinct Brevipalpus species. Aerial dispersal of Brevipalpus and its extensive host-plant tolerance (Childers and Rodrigues 2011, Childers et al. 2003) could be 2 primary factors that explain the pervasiveness of this genus locally. Brevipalpus’ global distribution has been attributed to the active trade of ornamental species, via aerial dispersal (Kondo et al. 2006). When a host is near an uninfected ornamental species it may easily introduce Brevipalpus. Through the extensive worldwide trade in ornamental plants, Brevipalpus colonization can now spread to different areas across the globe. The island of Puerto Rico has an active ornamental plant industry (Alamo et al. 2004), so it will be important to investigate the extent to which these species are currently being imported to the island (vs. produced locally) and the extent by which Brevipalpus mites might be inadvertently introduced to the island through the trade in ornamental plants. Even when sustainable gardening practices focus on the use of native plants in gardening (Cross and Spencer 1996), Brevipalpus mites are likely to be a concern as exhibited in this study by the infestation of all native species. Research may be needed to identify appropriate native species that are resistant to pests. While evaluating additional native species for local landscaping may be a priority, one limitation may be the low frequency of native species in local commercial nurseries (Torres-Camacho et al. 2016). Brevipalpus mites have become an economic concern because of their potential negative effects on the agricultural sector (Alamo et al. 2004). On a small island, such as Puerto Rico, this species could easily become a pest that destroys agricultural crops and ornamentals in city areas. Brevipalpus mite species are 9

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complex, resilient, and flexible organisms whose numbers can reach to millions within 1 single plant; these mites are relatively long-lived in comparison to those in other families, and hosts of Brevipalpus mites are infected for their lifetime once a mite-transmitted virus is established (Beard et al. 2015, Childers and Rodrigues 2005). In some cases, during severe outbreaks, entire orchards of a few hectares have been destroyed (Childers and Rodrigues 2011). Our study did not focus on viruses associated with Brevipalpus species; however, we observed symptoms like those associated with viruses (chlorotic spots, coffee ringspot, and citrus leprosis) on all the plants that hosted Brevipalpus (A.L. Henderson, pers. observ.). To the extent that the occurrence of Brevipalpus is linked to viral plant diseases (Childers and Rodrigues 2011), we recommend monitoring the affinity of Brevipalpus with different plant species and the role of the ornamental plant trade to the local spread of Brevipalpus. Acknowledgments We thank all of the homeowners who welcomed us and granted permission to remove ornamental leaves from their yards. We also appreciate Cristina Vila-Ruiz, who assisted in field sampling and identification of plants, and José Carlos Rodrigues’ lab group for fruitful conversations and assistance with Brevipalpus identification. We offer a special thanks to Alonso Ramirez. This material was based upon work supported by the National Science Foundation under Grant No. DBI- 1062769 at El Verde Field Station and USDA-APHIS 8130-059 CA. Literature Cited Agrawal, A.A., J.A. Lau, and P.A. Hamback. 2006. Community heterogeneity and the evolution of interactions between plants and insect herbivores. The Quarterly Review of Biology 81(4):349–376. Alade, P.I., and O.N. Irobi. 1993. Antimicrobial activities of crude leaf-extracts of Acalypha wilkesiana. Journal of Ethnopharmacology 39:171–174. Alamo C.I., R.A. Franqui, and E. Evans. 2004. The economic impact of invasive species in the ornamental commodity in Puerto Rico: Towards establishing a multidemsional framework for data collection and analysis. International Agricultural Trade and Policy Center 4(2):1–13. Beard, J.J., R. Ochoa, W.E. Braswell, and G.R. Bauchan, 2015. Brevipalpus phoenicis (Geijskes) species complex (Acari: Tenuipalpidae): A closer look. Zootaxa 3944:1–67. Bobot, T.E., E. Franklin, D. Navia, T.R. Gasnier, A.C. Lofego, and B.M. Oliveira. 2011. Mites (Arachnida, Acari) on Citrus sinensis (L.). Osbeck Orange trees in the State of Amazonas, Northern Brazil. Acta Amazonica 41(4):557–566. Chagas, C.M., E.W. Kitajima, and J.C.V. Rodrigues. 2003. Coffee Ringspot virus vectored by Brevipalpus phoenicis (Acari: Tenuipalpidae) in Coffee. Experimental and Applied Acarology 30:203–213. Childers, C.C., and K.S. Derrick. 2003. Brevipalpus mites of unassigned rhabdovirus in various crops. Experimental and Applied Acarology 30:1–3. Childers, C.C., and J.C.V. Rodrigues. 2005. Potential pest mite species collected on ornamental plants from Central America at port of entry to the United States. Florida Entomologist 88(4):408–414. 10

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Childers, C.C., and J.C.V. Rodrigues. 2011. An overview of Brevipalpus mites (Acari: Tenuipalpidae) and the plant viruses they transmit. Zoosymposia 6:180–192. Childers, C.C., J.C.V. Rodrigues, and W.C. Welbourn. 2003. Host plants of Brevipalpus californicus, B. obovatus, and B. phoenicis (Acari: Tenuipalpidae) and their potential involvement in the spread of viral diseases vectored by these mites. Experimental and Applied Acarology 30:29–105. Chong, J.H., R.D. Oetting, and L.S. Osborne. 2005. Development of Diomus austrinus Gordon (Coleoptera: Coccinellidae) on two mealybug-prey species at five constant temperatures. Biological Control 33(1):39–48. Cross, R., and R. Spencer. 1996. Sustainable gardens. CSIRO Publishing, Collingwood, Australia. 342 pp. Gurevitch J., S.M. Scheiner, and G.A. Fox. 2002. The Ecology of Plants. Sinauer Associates, Sunderland, MA, USA. 518 pp. Hogendorp, B.K, R.A. Cloyd, and J.M. Swiader. 2006. Effect of nitrogen fertility on reproduction and development of Citrus Mealybug, Planococcus citri (Risso) (Homoptera: Pseudococcidae), feeding on two colors of Coleus, Solenostemon scutellarioides L. Codd. Environmental Entomology 35(2):201–211. Kitajima, E.W., J.A.M. Rezende, and J.C.V. Rodrigues. 2003. Passion Fruit Green Spot virus vectored by Brevipalpus phoenicis (Acari: Tenuipalpidae) on Passion Fruit in Brazil. Experimental and Applied Acarology 30:225–231. Kitajima, E.W., J.C.V. Rodrigues, and A.J. Freitas. 2010. An annotated list of ornamentals naturally found infected by Brevipalpus mite-transmitted viruses. Scientia Agricola 67(3):348–371. Kondo, H., T. Maeda, and T. Tamada. 2003. Orchid Fleck virus: Brevipalpus californicus mite transmission, biological properties, and genome structure. Experimental and Applied Acarology 30:215–223. Kondo, H., M. Takanori, Y. Shirako., and T. Tamada. 2006. Orchid Fleck virus is a rhabdovirus with an unusual bipartite genome. Journal of General Virology 87:2413–2421. Krantz, G.W. 2009. Habits and habitats. Pp. 64–82, In. G.W. Krantz and D.E. Walter (Eds.) A Manual of Acarology. Texas Tech University Press, Lubbock, TX, USA. 807 pp. Lim, S.W., K.N. Ting, T.D. Bradshaw, N.A. Zeenathul, C. Wiart, T.J. Khoo, K.H. Lim, and H.S. Loh. 2011. Acalypha wilkesiana extracts induce apoptosis by causing single-strand and double-strand DNA breaks. Journal of Ethnopharmacology 138(2):616–623. Lugo, A.E., O. Ramos, and C. Rodríguez-Pedraza. 2011. Description of the Río Piedras River Watershed and its surrounding environment. International Institute of Tropical Forestry, USDA Forest Service, Jardín Botánico Sur, San Juan, PR, USA. Meléndez-Ackerman, E.J., C.J. Nytch, L.E. Santiago-Acevedo, J.C. Verdejo-Ortiz, R. Santiago-Bartolomei, L.E. Ramos-Santiago, and T.A. Muñoz-Erickson. 2016. Synthesis of household yard-area dynamics in the city of San Juan using multi-scalar socialecological perspectives. Sustainability 8:481. Miranda, L.C., D. Návia, and J.C.V. Rodrigues. 2007. Brevipalpus mites Donnadieu (Prostigmata: Tenuipalpidae) associated with ornamental plants in Distrito Federal, Brazil. Acarology. Neotropical Entomology 36(4):587–592. Návia, D., R.S. Mendonça, F. Ferragut, L.C. Miranda, R.C. Trincado, J. Michaux, and M. Navajas. 2013. Cryptic diversity in Brevipalpus mites (Tenuipalpidae). Zoologica Scripta 42(4):406–426. Ramos-González, O.M. 2014. The green areas of San Juan, Puerto Rico. Ecology and Society 19(3):21. 11

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