AnimaliaHymenopteraFormicidaeMesserSteven J.CoverStefan P.LaPollaJohn S.Nylanderia deceptrix sp. n., a new species of obligately socially parasitic formicine ant (Hymenoptera, Formicidae)Zookeys13120162016552496510.3897/zookeys.552.6475 Nylanderia deceptrix http://zoobank.org/B5A11117-4638-4B6D-9908-6208C05CF558 sp. n.Figs 2, 3 (queen); 4–11 (male)Holotype

queen, USA. Massachusetts: Plymouth County: Myles Standish State Forest; Southeast Line Road; 41°49.12'N, 70°39.75'W; elev. 31 m; in Nylanderia parvula nest; 06 June 2013 (S. Messer) (MCZC); 10 paratype queens and 7 paratype males same locality information as holotype except different collection dates (MCZC and USNM).

Diagnosis.

Queen: smallest of Nearctic Nylanderia (TL less than 3.5 mm); mesosoma color mottled with areas of lighter and darker brown to yellowish-brown; Male: very small, nonfunctional wings present.

QUEEN. Measurements (n=10): TL: 2.91–3.40; HW: 0.55–0.63; HL: 0.58–0.69; EL: 0.22–0.24; SL: 0.73–0.78; MW: 0.52–0.57; PW: 0.55–0.67; WL: 0.99–1.07; GL: 1.24–1.69; PDH: 0.35–0.42; PFL: 0.67–0.72; PFW: 0.15–0.17; SMC: 0–3; PMC: 4–5; MMC: 21–27; MtMC: 3–4.

Indices: CI: 92–97; REL: 33–37; SI: 121–130; FI: 21–24.

Overall brown to yellowish-brown; head and gaster darker brown with generally lighter mesosoma; mesosoma color mottled with areas of lighter and darker brown to yellowish-brown; antennae, mandibles and legs yellow; body covered with dense pubescence; macrosetae dark brown but usually with lighter yellowish-brown tips. Eyes bulge slightly beyond head outline in full-frontal view; three prominent ocelli present. Scapes long; yellow; exceed posterior margin of the head by the length of first 3 funicular segments; scapes with dense pubescence and sometimes with up to three short standing macrosetae, but often with none. Head with abundant macrosetae and layer of pubescence; slightly longer than broad; becoming slightly wider at posterior of head. Mesosoma covered with erect macrosetae and pubescence; most macrosetae on mesonotum and metanotum show strong curvature. Gaster covered in pubescence and a large cluster of macrosetae on first gastral tergite.

MALE. Measurements (n=5): TL: 1.91–2.05; HW: 0.45–0.46; HL: 0.48–0.53; EL: 0.17–0.18; SL:0.57–0.59; MW: 0.28–0.32; PW: 0.37–0.39; WL: 0.66–0.69; GL: 0.74–0.88; PDH: 0.24–0.26; PFL: 0.52–0.54; PFW: 0.11–0.13; PL: 0.20–0.24; SMC: 0; PMC: 0; MMC: 7–12; MtMC: 1–2.

Indices: CI: 88–97; REL: 34–36; SI: 125–127; FI: 22–25.

Overall color brown to brownish-yellow; head and gaster darker brown with generally lighter mesosoma; antennae, mandibles, legs, and parameres yellow; body covered with dense pubescence; macrosetae dark brown but usually with lighter yellowish-brown tips; cuticular surface dull, covered in a dense layer of appressed setae. Head longer than broad; eyes large and bulging beyond head outline in full-frontal view; three prominent ocelli present; scapes long, exceeding posterior margin of the head by length of first 3 funicular segments; scapes absent of macrosetae and with a dense layer of pubescence; clypeus roughly rectangular, with anterior margin emarginated; mandible broad, with 4 teeth; all but apical tooth are weakly developed; apical tooth distinct, curves in toward body midline. Mesosoma relatively small; very small nonfunctional wings present; mesosoma covered in pubescence, with erect setae of varying lengths dorsally and on legs. Pronotum collar-like; mesonotum offset from pronotum at sulcus; mesonotum rises sharply above height of pronotum; mesonotum flat dorsally with many erect setae of varying lengths; marcosetae on mesonotum and metanotum show strong curvature of about 90°; propodeum indistinct from remainder of mesosoma, but with steep declivity; petiole short, triangular, upright, with posterior face only slightly longer than anterior face. Gaster with a dense layer of pubescence and erect setae; parameres especially setose; parameres roughly triangular, turning slightly mesad posteriorly; long setae extend off of parameres; cuspi small and tubular, reaching digiti dorsally; digiti weakly anvil-shaped, with poorly developed point directed ventrally; volsellar lobes flat, slightly indented relative to digital margin.

Etymology.

The species epithet deceptrix (Latin = deceiver) is attributed to the parasitic lifestyle, deceiving the host to allow cohabitation.

Notes.

Nylanderia deceptrix can be identified from other Nearctic species because it has the smallest queens of all Nearctic Nylanderia, ranging between 2.91–3.40 mm (Trager 1984, Kallal and LaPolla 2012). Compared to other Nearctic species with no macrosetae on the scape such as Nylanderia parvula and Nylanderia trageri (Kallal and LaPolla 2012), Nylanderia deceptrix is the only species with queens showing bicoloration, with the head and gaster being darker in color than the mesosoma. Additionally the queens have a mottled coloration on the mesosoma with areas of darker brown and yellow-brown. Nylanderia deceptrix males are currently the only Nearctic Nylanderia to display highly reduced wings. The male parameres display dense and very long macrosetae compared to those of other Nearctic species. The digitus displays a narrower area towards the base of the structure that expands towards the tip and ends with a narrow point. The end of the digitus also has distinct foveolate (pitted) sculpturing. The head of both the queen and the male are worker-like in overall appearance (except for the presence of distinct, large ocelli; never strongly developed in workers), and are longer than wide, whereas Nylanderia reproductives, especially queens, typically have wider than long heads. Additionally, Nylanderia queens usually have heads covered in dense pubescence, and this is not the case in Nylanderia deceptrix.

Prevalence of host species and parasitism rate.

Across the seven transects, the average Nylanderia parvula nest entrance density was 2.35 nest entrances/m2 (SD=0.15), ranging from 1.64–2.64 nest entrances/m2 for the individual transects. Transect 1 was excluded from all calculations because of inexperience in locating nest entrances and insufficient surveying effort resulting in a density 81.3% less than the average across all other transects.

In total, 356 Nylanderia parvula colonies were excavated and checked for the presence of Nylanderia deceptrix. Of those 356 colonies, nine had Nylanderia deceptrix present, resulting in a parasitism rate of 2.53%. The number of Nylanderia deceptrix queens found in a single colony ranged from 1–8 per colony. Nylanderia deceptrix males were only found in one of the nine parasitized colonies, and contained a total of nine males. Nylanderia deceptrix brood were found in two of the nine parasitized colonies. One colony contained only a single Nylanderia deceptrix queen pupa. The range for Nylanderia parvula pupal length was 3.31–3.89 mm (n=84) and the range for Nylanderia deceptrix pupal length was 2.73–3.20 mm (n=30). On the other end of the spectrum one colony contained 74 Nylanderia deceptrix queen pupae and 4 Nylanderia deceptrix male pupae (male Nylanderia deceptrix pupae could be determined by highly reduced wing buds and the presence of genitalia).

Reproductive cycle.

All colonies that were found to have dealate queens (n=17) only possessed one queen and we are taking this as evidence of monogyny in Nylanderia parvula. A total of 43 colonies were excavated and used for population census data collection. Among the 43 colonies, the average number of adult Nylanderia parvula reproductives (alate queens and males) found in colonies was: 15.4 (±23.3) for May, 0 for June, 6.1 (±4.1) for July, and 20.4 (±11.77) for September (Fig. 12). Compared to the number of alates, the total brood (larvae and pupae combined) within colonies shows the opposite trend (Figs 12, 13). Counts were low in May (37 ±134.2) and September (15.8 ±209.6), moderate in July (177.6 ±65.2), and at the highest in June (722.7 ±116.1). Nylanderia parvula reproductive pupae were only found in July, and Nylanderia deceptrix reproductive pupae were only observed in July as well.

Box-and-Whisker plot of within colony Nylanderia parvula alate reproductive counts from May, June, July and September.

Box-and-Whisker plot of within colony Nylanderia parvula brood counts from May, June, July and September.

Flight and dispersal.

Forewing length

(FWL) measurements were used along with Weber’s Length to determine a ratio of forewing to Weber’s length to examine if the wings of Nylanderia deceptrix were smaller in proportion to Nylanderia parvula. The FWL:WL for Nylanderia parvula ranged from 2.27–2.59, with an average of 2.47 (±0.018), and for Nylanderia deceptrix the ration ranged from 2.07–2.31, averaging 2.18 (±0.014). Comparing the averages using a Student’s t-test, the difference between the two was significant (P<0.00001, t=12.59 for a two-tailed test), meaning the wings of Nylanderia deceptrix were smaller in proportion to Weber’s length compared to Nylanderia parvula. When examining the scatter plot of Weber’s length to forewing length of all the Nylanderia species used (see material and methods for list), Nylanderia deceptrix falls well below the trendline created from the data of the other species (Fig. 14). The R2 value of the trendline was significant with a P-value<0.00001 (F=98.12), indicating a true relationship between forewing length and Weber’s length for the non-obligately socially parasitic Nearctic Nylanderia species.

Scatter plot displaying mesosoma length (=Weber’s length) to forewing length and trendline fitting non-parasitic Nearctic Nylanderia: Nylanderia arenivaga, Nylanderia austroccidua, Nylanderia concinna, Nylanderia faisonensis, Nylanderia parvula, Nylanderia phantasma, Nylanderia querna, Nylanderia terricola, Nylanderia vividula, and Nylanderia wojciki (diamonds) with added Nylanderia deceptrix data (squares, not part of trendline data).

Both Nylanderia deceptrix and Nylanderia parvula queens were allowed to climb to the top of a pencil to see if they would use it as a location to take off and fly from. Five Nylanderia parvula queens were tested and each of them flew off of the pencil tip within two trials, however, none of the five Nylanderia deceptrix flew off of the pencil tip after five trials for each individual. In the lab, attempts at dropping two Nylanderia deceptrix queens over a white surface to provoke flight while freefalling were conducted, but neither of them flew. As Nylanderia deceptrix individuals were hard to collect and maintain in a laboratory setting; only two drop trials were done per individual to avoid harming or losing individuals.

Aggression.

The aggression tests between workers, the pairing of both Nylanderia parvula workers from not parasitized colonies had an average score of 2.5 (n=6, range 1–3), from one parasitized and one not parasitized colony averaged 4.4 (n=5, range 3–5), and from both parasitized colonies averaged 2.67 (n=3, range 1–4) (here colony is always referring to Nylanderia parvula colonies). Pairings with an Nylanderia deceptrix queen and a Nylanderia parvula worker from a not parasitized colony had an average of 5 (n=2), and with a Nylanderia parvula worker from a parasitized colony averaged 1 (n=2). Also, the average aggression between a Nylanderia deceptrix queen and a Nylanderia parvula queen was 1.88 (n=16, range 1–3). Introduction tests placing a Nylanderia parvula worker from a parasitized colony into another parasitized colony had an average score of 3.33 (n=3, range 2–5), and introducing a Nylanderia deceptrix queen to an already parasitized colony averaged 2.33 (n=3, range 1–5). Two of the three Nylanderia deceptrix introductions into an already parasitized colony resulted in acceptance of the queen into the new colony (score=1), while the third was attacked and rejected (score=5). When taking Nylanderia deceptrix queens or parasitized colony workers and introducing them to not parasitized colonies, the average score was 5 for each case (n=4 and 5, respectively). Similarly, workers from not parasitized colonies introduced to a parasitized colony resulted in an average score of 4.75 (n=4). The final set of introductions involved taking a Nylanderia parvula worker from a not parasitized colony and introducing her to another not parasitized colony. The resulting average score for that case was 4.8 (n=5, range 4–5). See Table 1 for all the aggression and introduction test average scores.

Average Aggression scores (see text for details) for aggression and introduction tests (n=sample size). W/W-Colony

= Nylanderia parvula worker to Nylanderia parvula worker

; Dec/W-Colony

= Nylanderia deceptrix queen to Nylanderia parvula worker

; Dec/Queen

= Nylanderia deceptrix queen to Nylanderia parvula queen

.

W/W-Colony (N) Dec/W-Colony (N) Dec/Queen (N)
Parasitized to Parasitized
Solo Aggression 2.67 (3)1 (2)---
Introduction Test 3.33 (3)2.33 (3)---
Parasitized to Not Parasitized
Solo Aggression 4.4 (5)5 (2)1.88 (16)
Introduction Test 5 (5)5 (4)---
Not Parasitized to Not Parasitized
Solo Aggression 2.5 (6)------
Introduction Test 4.8 (5)------
Not Parasitized to Parasitized
Introduction Test 4.75 (4)------

Nylanderia deceptrix (queen USNMENT00755074; male 4, 5 USNMENT00755083; male 6–11 USNMENT00755073): 2 queen in lateral view 3 queen head in full-frontal view 4 male in lateral view 5 male head in full-frontal view 6–9 male genitalia in dorsal, lateral, and ventral view, and ventral view close-up of digitus and cuspis 10 male 9th sternite 11 penis valve (ectal view).

TragerJC (1984) A revision of the genus Paratrechina (Hymenoptera: Formicidae) of the Continental United States. Sociobiology 9: 1162. KallalRJLaPollaJS (2012) Monograph of Nylanderia (Hymenoptera: Formicidae) of the World, Part II: Nylanderia in the Nearctic. Zootaxa 3508: 164.