Nylanderia fulva

Kumar et al. (2015) - The tawny crazy ant, Nylanderia fulva is invading the southern United States (Gotzek et al. 2012). Its occurrence in the United States (US) was first documented in Houston in 2002 (Meyers and Gold 2008). It may have arrived in Florida earlier (Klotz et al. 1995; Deyrup et al. 2000), but collections of the very similar Nylanderia pubens from Florida dating back to the 1950s (Trager 1984) prevent an accurate identification of early pest populations. At present, this species occurs in Texas, Florida, southern Mississippi (MacGown and Layton 2010) and southern Louisiana (Hooper-Bui et al. 2010; Fig. 1). Introduction of N. fulva in Colombia caused extensive ecological and agricultural damage (Zenner de Polania 1990). In the Southern United States, N. fulva displaces red imported fire ants (Solenopsis invicta), and regionally distributed native species, thereby reducing both biological and functional diversity (LeBrun et al. 2013). Nylanderia fulva can also transport pathogens of plants, humans, and other animals (McDonald 2012). Nests within populations contain multiple queens (Zenner de Polania 1990). Interconnected nests of these ants form extraordinarily dense populations that greatly exceed the combined densities of all ants in adjacent uninvaded assemblages (LeBrun et al. 2013). They feed on small insects and vertebrates, and honeydew secreted by aphids (Zenner de Polania and Bola~nos 1985). They invade people’s homes, nest in crawl spaces and walls, and damage electrical equipment resulting in millions of dollars of losses (Blackwell 2014). Populations spread about 200 m per year as a result of nest fission at the invasion front (Meyers and Gold 2008). Female reproductives of N. fulva have not been observed to engage in alate flights, so long-distance dispersal occurs largely as a result of human transport of nesting ants.

Identification
Fortunately recent revisionary taxonomic work with this genus and the clade of genera it belongs with by LaPolla and colleagues has brought new clarity and a much sounder understanding of Nylanderia species delineations. N. fulva though remains a problematic species. As per Gotzek et al (2012): A recent phylogeny placed this particular species within a clade of mostly undescribed species of South American and Caribbean crazy ants.

Identification Keys including this Taxon

 * Key to Nearctic Nylanderia workers
 * Key to Nearctic Nylanderia males

Distribution
Known from numerous locations throughout the neotropics, and beyond, but identification of this and similar Nylanderia suggest published accounts about this species are potentially suspect.

Distribution based on Regional Taxon Lists
Nearctic Region: Canada, United States. Neotropical Region: Argentina, Bolivia, Brazil, Chile, Colombia, Cuba, Dominican Republic, Ecuador, French Guiana, Grenada, Guyana, Haiti, Mexico, Paraguay, Suriname, Uruguay.

Biology
The following text and map are from Gotzek et al. (2012). References that were indicated but removed from the text are stated in the original publication:

There has been widespread misidentification of Nylanderia fulva. Within museum collections, misidentifications are common given the morphological similarities of the workers within the genus overall, as well as because of uncertainties regarding species boundaries.

Using a number of determination methods, it has been shown that this is the species that has experienced a population explosion in and around Houston, Texas that began in 2002 (Rasberry Ant).

Since its detection in Harris County, Texas, the new invasive has rapidly expanded its range and is now found in 21 counties in southeast Texas and has recently been discovered from southwestern Mississippi and Louisiana (see Figure).

Figure 1. Reported distribution of the Rasberry Crazy Ant in the United States (in blue). The distribution of Nylanderia cf. pubens in Florida is given in orange, but we suspect that these may prove to be N. fulva. Counties highlighted with solid colors indicate verified occurrences, whereas hatched counties are unconfirmed reports. Red dots indicate collection sites for samples used in this study. The actual distribution of N. fulva in the United States is most likely to be more widespread. DOI:10.1371/journal.pone.0045314.g001

Given the uncertainty of workerbased identifications of N. fulva and N. pubens most publications that involve either of these species are suspect; they may not involve the species listed in the publication, including the possibility that they are neither N. fulva nor N. pubens and are an entirely different Nylanderia species. It appears at this time that N. pubens is restricted to the Caribbean region. This species has been reported to be relatively to be relatively common in southern Florida in the 1950’s –1970’s, where it was also most recently found in 1994 (M. Deyrup, pers. comm. to JSL). It is not known whether these populations still persist today. Since we show that samples from northern Florida initially considered to be N. cf. pubens are actually N. fulva and given the invasive nature of N. fulva, we hypothesize that most or even all alleged occurrences of N. pubens in Florida are misidentified N. fulva. This would not be surprising, since the distribution is solely based on worker identifications (D. Oi, pers. comm. to DG). We also suspect that N. pubens may not have good invasive capabilities compared to N. fulva, given the currently rapidly expanding distribution of N. fulva in the United States and lack of N. pubens in our samples from northern Florida. It will require much better sampling of molecular data or male samples from throughout Florida to test our hypothesis. Currently, the Caribbean is likely the only place where N. fulva and N. pubens are sympatric and therefore the only region where identifications of workers will be difficult. If we are correct concerning the distribution and inability of N. pubens to become a pest, then the population explosions attributed to N. pubens that plagued the Caribbean from 19th century Bermuda to the recent outbreak on St. Croix and in southern Florida may very well have been N. fulva instead of N. pubens. Nylanderia fulva is known to be an invasive ant, most recently from Colombia where an outbreak occurred after this species was apparently introduced to control leafcutter ants and venomous snakes.

Therefore outbreaks may be common in N. fulva and should be expected in all inhabited areas, at least in the putative invasive part of its range. The current reported distribution of N. fulva in the United States is still patchy, but the pattern suggests that it will be able to invade the entire Gulf Coast, if it has not already done so. To accurately predict its potential range will require more detailed descriptions of its ecology, natural history, and distribution in its native range which can then be used to inform predictive environmental niche modeling. However, the native range of N. fulva must first be identified and, ideally, the source population(s) of the invasive populations must also be known. While this information is still lacking, it is highly likely that N. fulva is native to South America, probably southern South America (the type locality is in Brazil). Like other notorious invasive ants, e.g., Solenopsis invicta or Linepithema humile, it is possible that N. fulva could be yet another ant from the greater Parana drainage that has become invasive elsewhere. Detailed phylogeographic and population genetic studies based on broad and extensive sampling across the entire range of the species will help address these issues and provide the basis for effective management of N. fulva in North America, for example through the introduction of co-evolved biological control agents.

Research can now focus on this species’ population dynamics, ecology, natural history, and identification of its native range to better understand the causes and consequences of such rapid population growth. This endeavor would not have been possible without the collection-based resources and taxonomic expertise present in natural history museums, underscoring their value for both basic and applied research.

Eyer et al. (2018) highlighted a shift in colony structure following invasion. In its native range, colonies are separated from one another, whereas no boundaries between nests are found in its invasive range. This genetic result is confirmed by a lack of aggression towards conspecifics. This suggests that N. fulva forms a single supercolony spreading more than 2000km covering its entire invasive range. This social structure provides several advantages in terms of colony growth, density, productivity and survival, and favors its invasive success outcompeting native species through resource monopolization. Drastic genetic differences between males and females might stem from a distortion of segregation, with queens preferentially transmitted paternal alleles to their sons and maternal ones to their daughters. As a consequence, the sexually produced female castes are highly heterozygous as they always inherited different alleles from their mother and father. This strategy allows N. fulva to maintain heterozygosity and overcomes the depletion of genetic diversity resulting from the founder event.

Brazil
DaRocha et al. (2015) studied the diversity of ants found in bromeliads of a single large tree of Erythrina, a common cocoa shade tree, at an agricultural research center in Ilhéus, Brazil. Forty-seven species of ants were found in 36 of 52 the bromeliads examined. Bromeliads with suspended soil and those that were larger had higher ant diversity. Nylanderia fulva was found in 18 different bromeliads but was associated with twigs and bark cavities, rather than suspended soil or litter, of the plants.

Chemical Ecology
LeBrun et al. (2015) found a behaviour, first noted and resulting from interactions between Solenopsis invicta and N. fulva, that detoxifies fire ant venom is expressed widely across ants in the subfamily Formicinae:

Solenopsis invicta is one of twenty exclusively New World fire ants, a subgroup of species within the large genus Solenopsis characterized by large, aggressive colonies of polymorphic workers with piperidine alkaloid-based venom (Blum 1992). Nylanderia fulva detoxifies S. invicta venom by applying its own venom, formic acid, to body parts exposed to S. invicta venom, using a prescribed series of stereotyped actions, or acidopore grooming. Standing on its hind and middle legs, the worker curls its gaster underneath its body. It then touches its acidopore (specialized exocrine-gland duct located at the gaster tip, uniquely shared among formicines) to its mandibles, runs its front legs through its mandibles, and grooms itself vigorously by rubbing its legs over its body, periodically reapplying its acidopore to its mandibles. Acidopore grooming by N. fulva results in greatly increased survivorship following conflict with fire ants or artificial exposure to fire ant venom (LeBrun et al. 2014). Although it is not yet demonstrated how formic acid alters the bioactivity of fire ant venom, formic acid protonates the nitrogen in fire ant venom alkaloids forming a protic ionic liquid with distinct physical properties (Chen et al. 2014). Among changes to the venom including the denaturation of associated venom enzymes and an increase in viscosity, the formate salt of the alkaloid is more polar and less lipophilic, which may reduce the ability of the protonated alkaloid to penetrate the waxy cuticle or cell membranes (Meinwald 2014). In addition to fire ant venom detoxification, the toxicity of formic acid itself is reduced as a result of salt formation. Acidopore grooming provides an effective mechanism for detoxification because, in conflicts with other ants, fire ants primarily apply venom topically by gaster flagging (a venom dispersal behavior) and smearing or flicking venom droplets exuded on the tips of their stingers onto competitors (Obin and Vandermeer 1985).

The specific chemistry of the reaction of formic acid with venom alkaloids and its use when challenged with specific venom types indicates that alkaloid venoms are targets of detoxification grooming. Solenopsis thief ants, and Monomorium species stand out as brood-predators of formicine ants that produce piperidine, pyrrolidine, and pyrroline venom, providing an important ecological context for the use of detoxification behavior. Detoxification behavior also represents a mechanism that can influence the order of assemblage dominance hierarchies surrounding food competition. Thus, this behavior likely influences ant-assemblages through a variety of ecological pathways.

Zhang et al (2015) discovered the interaction of Dufour’s gland secretion and formic acid from the venom gland was a potent recruitment communication in Nylanderia fulva. They suggested "Such recruitment via airborne volatiles from two separate glands is evidently an efficient mechanism enhancing both cooperative exploitation of large food items and the ability to marshal mass attack against enemies. This type of synergistic recruitment may also explain why N. fulva workers sometimes accumulate in massive numbers in electrical equipment. The initial response to outdoor electrical devices may simply be due to warmth, but short circuiting could create a snowball effect, whereby electrical and physical stimulation leads to ever more Dufour’s gland and venom gland discharge resulting in a much more dramatic response."

Endoparasites
Plowes et al. (2015) discovered the microsporidia Myrmecomorba nylanderiae in adult N. fulva.

Nomenclature

 *  fulva. Prenolepis fulva Mayr, 1862: 698 (w.q.) BRAZIL. Forel, 1891b: 94 (m.); Forel, 1912i: 67 (m.). Combination in Pr. (Nylanderia): Forel, 1908b: 67; in Paratrechina (Nylanderia): Emery, 1925b: 222; in Nylanderia: Kempf, 1972a: 166; in Paratrechina: Snelling, R.R. & Hunt, 1976: 122; in Nylanderia: LaPolla, Brady & Shattuck, 2010a: 127. Senior synonym of fumata: Wild, 2007b: 45. See also: Fernández, 2000: 146; Fox, et al. 2010: 795. Current subspecies: nominal plus biolleyi, cubana, fumatipennis, incisa, longiscapa, nesiotis.
 * fumata. Prenolepis fulva var. fumata Forel, 1909a: 264 (w.) PARAGUAY. Forel, 1912i: 67 (q.). Combination in Pr. (Nylanderia): Forel, 1913l: 246; in Paratrechina (Nylanderia): Emery, 1925b: 222; in Nylanderia: Kempf, 1972a: 166; in Paratrechina: Brandão, 1991: 366; in Nylanderia: LaPolla, Brady & Shattuck, 2010a: 127. Junior synonym of fulva: Wild, 2007b: 45.

Worker
Lange: 3.1 – 3.5mm. Gelbbraun, glanzend, Mandibeln, Geissel, Beine und besonders die Gelenke der Beine und die Tarsen heller. Mandibeln langsgestreift. Clypeus fast glatt, vorne nicht ausgerandet. Kopf seicht und zerstreut runzlig punctirt. Thorax fein runzlig punctirt, ebenso der Hinterleib, Scheibe des ersteren fast glatt. Schuppe oben abgerundet.

Queen
Lange: 6mm. Rothbraun, Gelenke der Beine und Tarsen gelb. Anliegende Pubescenz am Hinterleibe reichlich. Clypeus glanzend, fast glatt. Kopf, Thorax und Hinterleib fein runzlig punctirt. Schuppe oben ausgerandet.

Type Material
Rio Janeiro (Novara).