Honeydew-producing hemipterans in Florida associated with Nylanderia fulva (Hymenoptera: Formicidae), an invasive crazy ant.
Mutualisms between ants and honeydew producing hemipterans (e.g., aphids, scales, mealybugs, leafhoppers) are well-documented. Ants benefit from their association with hemipterans because their honeydew is an important source of carbohydrates (Stout 1979; Anderson & McShea 2001; Moya-Raygoza & Larsen 2008; Vanek & Potter 2010). Furthermore, hemipterans can serve as a protein resource if they are directly consumed by ants (Rosengren & Sundstrom 1991; Sakata 1994; Gullan 1997).
Conversely, hemipterans that produce honeydew benefit when they are tended by ants. Ants protect hemipterans from natural enemies and they sometimes provide them shelter (Sheppard et al. 1979; Stout 1979; Anderson & McShea 2001; Moya-Raygoza & Larsen 2008; Vanek & Potter 2010), thus allowing more hemipterans to survive and reproduce (Fritz 1982; Bristow 1983; Fowler & MacGarvin 1985; Buckley 1987). In addition, hemipterans that live inside ant nests (e.g., root feeding aphids and soft scales) are protected from climatic extremes (Buckley 1987). Some ants have been reported to assume parental care of hemipteran nymphs, enabling adult female hemipterans to produce more offspring (Bristow 1983). The removal of honeydew by ants may improve the hemipteran's environment by reducing the accumulation of sooty mold that grows on honeydew (Fokkema et al. 1983; Haines & Haines 1978). Sooty mold can suffocate hemipteran eggs (Moya-Raygoza & Nault 2000), affect crawler settling (Bess 1958), and cause adult mortality (Way 1954; Das 1959). In this study, we identified hemipteran species that were associated with N. fulva and documented N. fulva foraging activity with seasonal hemipteran abundance.
MATERIALS AND METHODS
Hemipterans Associated with Nylanderia fulva
From Jul to Oct 2010, colonies of N. fulva were observed in parks, natural areas and neighborhoods in Gainesville (Alachua Co.), Florida, for any tending behavior towards natural infestations of hemipterans on trees, shrubs and other plants. Nylanderia fulva trails on plants were visually followed until ants were seen tending individual hemipterans. Leaves or stems with the hemipterans were collected and insects and plants were identified by specialists at the Florida Department of Agriculture and Consumer Services, Division of Plant Industry (FDACS/DPI).
Nylanderia fulva populations and honeydewproducing hemipterans were monitored monthly from Feb 2011 to Jul 2012 at 3 sites in Gainesville, Florida. Four plant species [live oak (Quercus virginiana Mill.; Fagales: Fagaceae), holly (Ilex cornuta Lindl.; Aquifoliales: Aquifoliaceae), magnolia (Magnolia grandiflora L.; Magnoliales: Magnoliaceae) and sugarberry (Celtis laevigata Willd.; Urticales: Ulmaceae)] that were infested with at least 1 honeydew-producing hemipteran species, and had trails of N. fulva going up the stem were selected for monitoring. Four plants of each species were sampled except for magnolia, for which only one plant was sampled in 2011 and 3 more plants were added in 2012. The selected plant species were all located in managed landscapes, usually along driveways. Six to 10 terminal shoots per plant with at least 6 to 10 leaves were arbitrarily chosen, cut with a pole pruner and transported in plastic bags to the laboratory on ice. The total number of honeydew-producing insects on terminal shoots was counted within 24 h of collection.
Nylanderia fulva activity was estimated in 3 ways for each plant. First, a slice of sausage (0.5 x 2.5 cm Armour Original Vienna Sausage, Cherry Hill, New Jersey) was placed on the center of an index card (7.6 x 12.7 cm) that was positioned about 25 cm from the base of the plant on the northern and southern sides. After 15 min, each card with ants was individually bagged, frozen and the number of ants per sausage was determined. Second, the number of N. fulva foraging trails going up one major trunk per plant from the ground was counted. Finally, the number of workers walking past a specific point (~30.5 cm above the ground) on the most active foraging trail was counted for 20 s. All sampling occurred between 0900-1500 h when the air temperature was > 21[degrees]C.
Pearson's correlation was used to examine the association between the total number of hemipterans on a shoot and the 20 s ant count. Due to the increased number of trails per trunk in the summer, the 20 s count was multiplied by the number of trails to provide an index of trailing intensity. Analysis of variance (ANOVA) was conducted to determine differences in 20 s ant counts from the most active ant trail among plant species and Tukey's HSD test was used to conduct a mean separation among plant species (R Development Core Team 2012).
EESULTS AND DISCUSSION
Hemipterans Associated with Nylanderia fulva
A total of 17 species from 7 families of honeydew-producing hemipterans were tended by N. fulva on 10 plant species (Table 1). We did not observe Nylanderia fulva exhibiting any obvious preference for any particular hemipteran species. Aphids and mealybugs were the most prevalent and had the greatest diversity of species, with 6 species of aphids and 5 species of mealybugs. Similar observations of greater species diversity for these 2 families have also been reported in previous studies. Zenner-Polania (1990) reported N. fulva tending whiteflies and scale insects in orange trees and mealybugs in rangeland grass, sugarcane and coffee berries. They also observed that the ants transported the hemipterans from infested to uninfested plants and protected the hemipterans from the predators by constructing protective shelters over the mealybugs.
We observed carton shelters on magnolia branches, where N. fulva had covered tulip-tree scales using soil and plant debris (Fig. 1). Shelters were also observed on the trunk and near the base of the trunk where there were pruning injuries. Nylanderia fulva also built carton shelters around Juniper aphids (Cinara juniperivora (Wilson); Aphididae) along a split on the trunk on Southern red cedar (Juniperous silicicola (Small); Pinales: Cupressaceae) (Fig. 2). The structures were built in such a way that ants had access to enter and exit those shelters. When the carton was broken apart, many N. fulva workers scrambled out of the shelters and the juniper aphids or tuliptree scales (Toumeylla liriodendri (Gmelin); Coccidae) that were previously covered were visible. Many ants, like Acropyga, Formica, Lasius, Odontomachus and Oecophylla, build protective shelters of soil and plant debris, or carton, over honeydew producing hemipterans (Wheeler 1910; Way 1963; Evans & Leston 1971). These shelters are thought to protect the hemipterans from adverse environments (Way 1963; Helms & Vinson 2002), thereby increasing hemipteran populations and the availability of honeydew for the ant colony (Dejean et al. 1997).
The hemipterans collected from plants that were sampled monthly from Feb 2011 to Jun 2012 are listed in Table 2. The predominant hemipteran species on each host plant were Florida wax scale, Ceroplastes floridensis Comstock (Coccidae), onholly; the aphid, Myzocallis puncata (Monell), on live oak; the tuliptree scale, Toumeyella liriodendri (Gmelin), on magnolia; and the Asian wooly hackberry aphid, Shivaphis celti Das, on sugarberry. Nylanderia fulva were observed tending 5 hemipteran species on live oak and 3 species on sugarberry. Two hemipterans were sampled from holly, and only one was on magnolia. Among the sampled tree species, live oak and sugarberry were large, mature trees while holly and magnolia were smaller and younger landscape plantings that were pruned (Table 2). Thus, the difference in plant age and architecture could have affected the diversity of herbivorous hemipterans.
Hemipteran populations were higher during the warmer months (May to Sep) and decreased as ambient temperatures dropped at the end of Oct (Figs. 3a-6a). Similar temporal patterns of hemipteran distribution have been reported by Barlow (1962) for Myzus persicae (Sulzer) (Aphididae) on potatoes, Macrosiphum euphorbiae (Thomas) (Aphidae) on tobacco, and by Dixon (1977) in walnut aphid, lime aphid, cereal aphids and black bean aphid. Stevens et al. (1998) found that the population of several ant species that were tending the honeydew producing hemipterans decreased in cooler months when hemipteran numbers declined and increased in warmer months when hemipterans returned.
Similarly, N. fulva activity was greater during the warmer months (e.g., May to Aug) on all 4 plant species (holly, love oak, magnolia and sugarberry). Figure 3c-6c shows the number of ants foraging on the sausage provided during the samplings. The average number of ants crossing a specific point in 20 s during the 16 mo period in 2011-2012 is presented in Figures 3d-6d. As the daily average temperature decreased in Oct and Nov (< 21[degrees]C), ant numbers declined slightly. When the temperatures cooled further in Dec and Jan (< 19[degrees]C), ant foraging decreased dramatically, suggesting that the N. fulva activity is largely dictated by temperature. Ants are poikilothermic, thus their foraging activity depends on different abiotic factors like relative humidity and soil temperature (Traniello 1989; Valenzuela-Gonzalez et al. 1995). Porter & Tschinkel (1987) reported that Solenopsis invicta foraging activity was limited due to low temperatures in several locations of southeastern United States. Nylanderia fulva's activity appeared to be less in 2012 than in 2011 during similar months (Figs. 3a,c,d-6a,c,d). This was possibly due to the lower average RH (< 30%) in 2012 than in 2011. In addition, the average precipitation for Dec to Apr was also lower in 2012 (3.6 cm) than in 2011 (7 cm). Holldobler & Wilson (1990) suggested that warmer temperatures may not be enough for high ant activity. A relatively humid environment may be needed to avoid desiccation and to resume their activities in the open. Therefore, lower humidity and rainfall might have contributed to reduced N. fulva abundance in 2012 as compared to similar time periods in 2011. Hemipteran population size (Figs. 3a-6a) was also lower in 2012 than in 2011. It was not clear from our sampling alone that hemipteran numbers were lower because of decreased ant abundance or vice versa. More research will be required to evaluate this relationship.
Significant positive correlations were found between the total number of ants (trailing intensity) and the number of hemipterans in holly (r = 0.57, P < 0.0001), magnolia (r = 0.63, P < 0.0001), live oak (r = 0.80, P < 0.0001) and sugarberry (r = 0.44, P < 0.0001) (Figs. 3b-6b). Trees with higher hemipteran populations had higher N. fulva trailing intensity (i.e., the number of trailing ants crossing a specific point in 20 s x number of trails). Trailing intensity over time differed significantly among the 4 plant species (Fig. 7). Magnolia had an average trailing intensity of 136 ants throughout the sampling period which was significantly higher than the 43 ants on live oak. The trailing intensity on sugarberry and holly were similar at 8 and 7 ants, respectively (Fig. 7). Greater N. fulva trailing on magnolia and live oak could be attributed to greater hemipteran diversity and abundance. Tuliptree scale in magnolia is present in all stages of development during the winter in southern states (Donley & Burns 1971) and even though most insect species found in live oak were present in warmer months, lace bugs were present throughout the year in areas with mild winters like Florida (Dreistadt & Perry 2006) providing a continuous supply of honeydew to N. fulva. In contrast, on holly and sugarberry hemipterans were found only during the warmer months (Jul to Oct), and as a deciduous tree, sugarberry was defoliated from Oct to Feb. Brightwell & Silverman (2011) determined that there were fewer Linepithema humile (Mayr) (Formicidae) nests around deciduous trees in fall, but were present around evergreen species Pinus taeda L. (Pinales: Pinaceae) throughout winter and successfully foraged in these trees even when ambient temperatures were below the minimum foraging threshold. This pattern of behavior may be similar for the deciduous trees in our study where N. fulva moved their nests away from sugarberry in the winter, thus reflecting the reduced number ants in sugarberry after Oct 2011 (Figs. 6a,c,d).
In this study, the activity periods of honeydew producing hemipterans and N. fulva were positively associated, which reflected the seasonal changes in temperatures. During the warmer months (May to Oct), the presence and abundance of hemipterans increased, which was associated with greater ant foraging. Our paper also documents that some species of honeydew producing hemipterans that were tended by N. fulva were apparently protected by shelters created by N. fulva. Thus, there is evidence of mutualism between N. fulva and honeydew-producing hemipterans. Understanding the seasonal phenology between honeydew-producing hemipteran species tended by N. fulva could be important in developing control strategies for this invasive ant. Controlling hemipteran species would remove a food resource of N. fulva and thus could help decrease the density of ants in the landscape.
Caption: Fig. 1. Intact and broken carton shelters showing tuliptree scale (Toumeyella liriodendri (Gmelin)) in magnolia (Magnolia grandiflora L.).
Caption: Fig. 2. Intact and broken carton shelters showing Juniper aphid (Cinara juniperivora (Wilson)) on Southern Red Cedar (Juniperus silicicola (Small)).
Caption: Fig. 3. a) Mean number of hemipterans collected from the shoots every month from holly in Gainesville from Feb 2011 to Jun 2012. b) Correlation between number of hemipterans and number of ants (trailing intensity) on holly (r = 57). c) Mean number of ants collected on sausage samples every month at the base of holly in Gainesville from Feb 2011 to Jun 2012. d) Mean trailing intensity (i.e. ants crossing a specific point in 20 s x number of trails) on holly from Feb 2011 to Jun 2012.
Caption: Fig. 4. a) Mean number of hemipterans collected from the shoots every month from live oak in Gainesville from Feb 2011 to Jun 2012. b) Correlation between number of hemipterans and number of ants (trailing intensity) on live oak (r = 0.80). c) Mean number of ants collected on sausage samples every month at the base of live oak in Gainesville from Feb 2011 to Jun 2012. d) Mean number of trailing intensity (i.e. ants crossing a specific point in 20 s x number of trails) on live oak from Feb 2011 to Jun 2012.
Caption: Fig. 5. a) Mean number of hemipterans collected from the shoots every month from magnolia in Gainesville from Feb 2011 to Jun 2012. b) Correlation between number of hemipterans and number of ants (trailing intensity) on magnolia (r = 0.63). c) Mean number of ants collected on sausage samples every month at the base of magnolia in Gainesville from Feb 2011 to Jun 2012. d) Mean number of trailing intensity (i.e. ants crossing a specific point in 20 s x number of trails) on magnolia from Feb 2011 to Jun 2012.
Caption: Fig. 6. a) Mean number of hemipterans collected from the shoots every month from sugarberry in Gainesville from Feb 2011 to Jun 2012. b) Correlation between number of hemipterans and number of ants (trailing intensity) on sugarberry (r = 0.44). c) Mean number of ants collected on sausage samples every month at the base of sugarberry in Gainesville from Feb 2011 to Jun 2012. d) Mean number of trailing intensity (i.e. ants crossing a specific point in 20 s x number of trails) on sugarberry from Feb 2011 to Jun 2012.
Caption: Fig. 7. Mean number of ants crossing a specific point in 20 s on different tree species shown by analysis of variance and mean separation by Tukey's HSD test. Standard error bars with different letters indicate significantly different values (P < 0.05) (R Development Core Team 2012).
We would like to thank the owners and managers of our study sites in Gainesville for their cooperation and patience. Drs. S. Halbert and I. Stocks (FDACS/ DPI) kindly provided species identifications. We appreciate the technical assistance provided by P. Ruppert, M. Poudel, T. Garrick, D. Sekora and S. Rachel during field sampling. Dr. G. Hodges (FDACS/DPI) reviewed an earlier draft of this manuscript. This research was funded by the Tropical and Subtropical Agricultural Research (TSTAR) grant (2010-34135-21096).
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SHWETA SHARMA (1), DAVID H. OI (2) AND EILEEN A. BUSS (1), *
(1) Department of Entomology and Nematology, University of Florida, Gainesville, FL 32611-0620, USA
(2) USDA, ARS, Center for Medical, Agricultural, and Veterinary Entomology (CMAVE), 1600 S.W. 23rd Drive, Gainesville, FL 32608, USA
* Corresponding author: E-mail: firstname.lastname@example.org
TABLE 1. HEMIPTERANS TENDED BY NYLANDERIA FULVA IN GAINESVILLE, FLORIDA, FROM JUL 2010 TO OCT 2010. Insect Species Family Scientific Name Common name Aleyrodidae Dialeurodes Citrus whitefly citri (Ashmead) * Aphididae Aphis craccivora Cowpea aphid Koch * Aphis vernoniae Thomas Chaitophorus Willow aphid vimincola Hille Ris Lambers Cinara juniperivora Juniper aphid (Wilson) Sanbornia juniperi Pergande Shivaphis celti Das * Asian wooly hackberry aphid Coccidae Ceroplastes Florida wax scale floridensis Neopulvinaria Cottony maple innumerabilis scale (Rathvon) Kermesidae Allokermes sp. Kermes scale Pseudococcidae Antonina graminis Rhodes grass (Maskell) * mealybug Antonina pretiosa Noxious bamboo Ferris * mealybug Dysmicoccus Pineapple mealybug brevipes (Cockerell) * Phenacoccus parvus Lantana mealybug Morrison * Palmicultor Bamboo mealybug lumpurensis (Takahashi) * Psyllidae Pachypsylla Hackberry petiole venusta gall psyllid (Osten-Sacken) Tingidae Corythucha Florida oak floridana lace bug Heidemann Insect Species Family Scientific Name Host plant Aleyrodidae Dialeurodes Ligustrum citri (Ashmead) * Aphididae Aphis craccivora Hemp sesbania Koch * Aphis vernoniae Thomas Chaitophorus Black willow vimincola Hille Ris Lambers Cinara juniperivora Southern red cedar (Wilson) Sanbornia juniperi Southern red cedar Pergande Shivaphis celti Das * Sugarberry Coccidae Ceroplastes Burford holly floridensis Neopulvinaria Virginia creeper innumerabilis (Rathvon) Kermesidae Allokermes sp. Live oak Pseudococcidae Antonina graminis St. Augustine grass (Maskell) * Antonina pretiosa Switch cane Ferris * Dysmicoccus Live oak brevipes (Cockerell) * Phenacoccus parvus Live oak Morrison * Palmicultor Switch cane lumpurensis (Takahashi) * Psyllidae Pachypsylla Sugarberry venusta (Osten-Sacken) Tingidae Corythucha Live oak floridana Heidemann * Indicates introduced hemipteran insects to U.S. TABLE 2. LIST OF TREES, SAMPLING LOCATIONS, INSECTS AND NUMBER OF LEAVES THAT WERE SAMPLED. Tree Site Mean Honeydew producers No. of tree leaves/ ht (m) branch Burford Site 1 0.76 Florida wax scale 6 holly (Ceroplastes (Ilex floridensis cornuta Comstock) Lindl.) Mealybug (Dysmicoccus texensis (Tinsley)) Live oak Site 1 4.27 Lace bug 10 (Quercus (Corythucha virginiana floridana Mill.) Heidemann) Aphids (Myzocallis puncata (Monell)) Kermes scale (Allokermes sp. (Cockerell)) Bullet gall (Disholcaspis quercusvirens (Ashm.)) Pineapple mealybug (Dysmicoccus brevipes (Cockerell)) Magnolia Site 2 2.29 Tuliptree scale (Magnolia Site 3 (Toumeyella 3 grandiflora liriodendri L.) (Gmelin)) Sugarberry Site 2 6.4 Asian wooly 10 (Celtis hackberry aphid laevigata (Shivaphis celti Willd.) Das) Flatid plant hopper Psyllid gall (Pachypsylla sp.)
Please note: Some tables or figures were omitted from this article.
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