Acromyrmex fowleri Rabeling, Messer, Lacau and Delabie, 2019

Rabeling, C., Messer, S., Lacau, S., do Nascimento, I. C., Jr., M. Bacci & Delabie, J. H. C., 2019, Acromyrmex fowleri: a new inquiline social parasite species of leaf-cutting ants from South America, with a discussion of social parasite biogeography in the Neotropical region, Insectes Sociaux 66, pp. 435-451 : 445-448

Acromyrmex fowleri Rabeling, Messer, Lacau and Delabie , NEW SPECIES

Zoobank record: http://zoobank.org/ D96C94C2-AF2D- 4543-965E−49AB99DFE6 52.

Holotype, alate gyne BRAZIL, Bahia, Ilhéus, Praia do Norte, 18 km N Ilhéus; S14.6197°, W039.0607°; elevation above sea level: 0 m; collection date: 27 November 1994, 07.00 h; col. Jacques Delabie; individual was collected from the drift line of the Atlantic Ocean on the beach. Presumably alates of A. fowleri participated in a predawn nuptial flight and drowned in the sea. The holotype is deposited at the Laboratório de Mirmecologia , Centro de Pesquisa do Cacau , Itabuna, Bahia, Brazil ( CPCD) and carries the unique specimen identifier No. ASUSIBR00000001.

Description, holotype gyne Measurements: TL 7.90, WL 2.47, HL 1.30, HW 1.45, IOD 1.59, ML 0.97, FLD 0.75, SL 1.59, EL 0.37, EW 0.33, PrW 1.38, FL 1.73, PL 0.52, PW 0.57, PPL 0.50, PPW 0.92, GL 2.15, CI 110, MI 73, SI 109. A small species of Acromyrmex fungus-growing ants (WL 2.47, TL 7.90) that is immediately recognizable as a social parasite due to its smaller body size and shiny integument. Mandibles (MI 73) and appendages (FL 1.73, SI 109) long relative to head and body size, respectively. Integument smooth and shiny, in part translucent, characteristic of the inquiline syndrome. Body surface, antennal scapes, and legs (except for tarsi) sparsely covered with pale, transversally flattened, appressed setae; only tarsi covered with semi-erect setae. Color uniformly light orange brown; anepisternum, scutellum, and masticatory margin of mandibles slightly darker, reddish-brown. Head head shape subquadrate, slightly wider than long (CI 110); lateral margins parallel to each other; posterior margin with median concavity; posterior and lateral margins with numerous distinct tubercles. Mandibles long and slender in full-face view; external margins sinuate; masticatory margins with 12 teeth; apical and preapical teeth distinctly larger, followed by five small teeth that are interspersed by smaller denticles; mandible surface smooth and shiny, not striate. Palp formula 4:2, representing the plesiomorphic condition of fungus-growing ants. Posterior margin of clypeus trapezoidal, broadly inserted between frontal lobes; anterior margin of clypeus shiny and median portion concave. Unpaired median clypeal seta short (0.09 mm), semi-erect, transversally flattened, only barely projecting over the anterior clypeal margin. Frontal lobes broadly rounded, fully covering condylar bulbs in full-face view; lateral margin of frontal lobe serrated with two distinct tooth-like projections. Frontal carinae extending towards the level of the ocelli, not forming a fully shaped antennal scrobe. Preocular carina forming a straight line in lateral view and traversing the area of the antennal scrobe by onethird of the scrobe’s width behind the level of the eye. Eyes large (EL 0.37, EW 0.33) and strongly convex. The three ocelli are small and embedded in the integument. Antennae with 11 segments. Antennal scapes long (SL 1.59, SI 109) with abundant, appressed setae, surpassing the posterior margin of the head by more than one-third of its length. Mesosoma Mesosoma slender with caste-specific modifications related to wing bearing. Dorsolateral pronotal spine long, slender, and sharply pointed in dorsal view. Ventrolateral pronotal spine reduced, triangular, with blunt, rounded tip. Dorsum of mesosoma smooth and shiny. Posterior margin of scutellum concave, but not distinctly bidentate. Bulla and meatus of metapleural gland not notably modified from the condition in the host species. Propodeal spines straight, slen- der, sharply pointed, projecting away from the propodeum at a 90° angle in lateral view. Metasoma Anterior peduncle of petiole short, about one-fourth the length of the petiolar node. Dorsum of petiolar node with a pair of irregularly shaped ridges. Postpetiole wider (PPW 0.92) than long (PPL 0.50) in dorsal view, posterior margin slightly concave. Gaster large (GL 2.15). First gastric tergite notably smooth with few broadly rounded, reduced tubercles; on median portion of anterior half tubercles form a pair of shallow, longitudinal ridges. Except for the smaller size, fore- and hindwings resemble the wings of the host species, A. rugosus .

Measurements, paratype gynes (n = 25): TL 7.33–8.13, WL 2.34–2.69, HL 1.25–1.31, HW 1.38–1.47, IOD 1.53–1.61, ML 0.89–0.98, FLD 0.73–0.78, SL 1.51–1.71, EL 0.36–0.39, EW 0.33–0.37, PrW 1.23–1.44, FL 1.65–1.76, PL 0.48–0.58, PW 0.56–0.63, PPL 0.43–0.55, PPW 0.91–1.02, GL 1.90–2.22, CI 106–114, MI 69–76, SI 107–120.

Paratypes 279 alate g y n e s a n d 8 4 m a l e s, ASUSIBR00000002-00000364 , from three collection sites along a 40 km stretch of “restinga” habitat (i.e., tropical and subtropical coastal forest habitats that form on sandy, acidic, nutrient-poor soils) along the coastline with the city of Ilhéus at its center .

First collection site: BRAZIL, Bahia, Ilhéus, Praia do Sul, STAC camping, 13 km south of Ilhéus; near the entrance of a subterranean nest of Acromyrmex rugosus dug in the sand about 100 m from the beach, S14.91210°, W039.02095°; elevation above sea level: 5 m; collection date: 29 October 1992; col. Jacques H. C. Delabie (1 alate gyne, ASUSIBR00000002); same as above, but 05 November 1992 (7 alate gynes and 6 males, ASUSIBR00000003-15); same as above, but 15 January 1993; col. Harold G. Fowler (1 alate gyne ASUSIBR00000016).

Second collection site: BRAZIL, Bahia, Ilhéus, Praia do Norte, Barramares village, 18 km north of Ilhéus, from the drift line of the Atlantic Ocean on the beach; S14.6197°, W039.0607°; elevation above sea level: 0 m; collection date: 01 November 1993; col Jacques H. C. Delabie (1 male, ASUSIBR00000017); same as above, but 06 November 1993 (2 males, ASUSIBR00000018-19); same as above, but 14 November 1993 (3 males, ASUSIBR00000020-22); same as above, but 13 December 1993 (1 male, ASUSIBR00000023); same as above, but 08 January 1994, 18:00 h (1 male, ASUSIBR00000024); same as above, but 14 January 1994 (2 alate gynes ASUSIBR00000025-26); same as above, but 06 February 1994, 08:00 h (1 alate gyne and 1 male, ASUSIBR00000027-28); same as above, but 06 March 1994, 07:00 h (1 alate gyne, ASUSIBR00000029); same as above, but 20 March 1994, 07:00 h (1 alate gyne, ASUSIBR00000030); same as above, but 01 April 1994, 07:00 h (1 alate gyne, ASUSIBR00000031); same as above, but 02 April 1994, 07:00 h (1 male, ASUSIBR00000032); same as above, but 21 May 1994, 08:00 h (1 male, ASUSIBR00000033); same as above, but 12 June 1994, 08:00 h; col. Ivan C. do Nascimento (1 alate gyne, ASUSIBR00000034); same as above, but 12 October 1994; col. Clayton R. R. Delabie (2 alate gynes and 2 males, ASUSIBR00000035-38); same as above, but 16 October 1994, 07:00 h; col. Clayton R. R. Delabie (1 alate gyne and 4 males, ASUSIBR00000039-43); same as above, but 29 October 1994, 07:00 h; col. Jacques H. C. Delabie and Clayton R. R. Delabie (17 alate gynes and 4 males, ASUSIBR00000044-64); same as above, but 13 November 1994, 07:00-08:00 h; col. Clayton R. R. Delabie (84 alate gynes and 9 males, ASUSIBR00000066-158); same as above, but 20 November 1994, 07:00 h; col. Clayton R. R. Delabie (1 alate gyne and 1 male, ASUSIBR00000159-160); same as above, but 24 November 1994 (1 alate gyne, ASUSIBR00000161); same as above, but 27 November 1994, 07:00 h (112 alate gynes and 26 males, ASUSIBR00000162-298); same as above, but 04 December 1994, 07:00 h (4 alate gynes and 1 male, ASUSIBR00000299-303); same as above, but 18 December 1994, 06:00 h; col. Clayton R. R. Delabie (2 alate gynes and 3 males, ASUSIBR00000304-308); same as above, but 27 December 1994, 07:00 h; col. Ivan C. do Nascimento (2 alate gynes and 2 males, ASUSIBR00000309-312); same as above, but 31 December 1994, 06:00 h; col. Clayton R. R. Delabie (1 alate gyne, ASUSIBR00000313); same as above, but 01 January 1995, 06:00 h; col. Clayton R. R. Delabie (3 alate gynes, ASUSIBR00000314-316); same as above, but 15 January 1995, 06:00 h (1 alate gyne, ASUSIBR00000317); same as above, but 19 January 1995, 07:00 h; col. Ivan C. do Nascimento (1 male, ASUSIBR00000318); same as above, but 27 January 1995 (1 male, ASUSIBR00000319); same as above, but 12 February 1995, 07:00 h (2 alate gynes, ASUSIBR00000320-321); same as above, but 26 February 1995, 06:00 h (1 alate gyne, ASUSIBR00000322); same as above, but 28 February 1995, 06:00 h (2 alate gynes and 1 male, ASUSIBR00000323-235); same as above, but 01 March 1995, 06:00 h (1 alate gyne and 1 male, ASUSIBR00000326-327); same as above, but 03 March 1995, 06:00 h (1 alate gyne and 2 males, ASUSIBR00000328-330); same as above, but 11 March 1995, 07:00 h (1 alate gyne, ASUSIBR00000331); same as above, but 17 March 1995, 07:00 h (1 alate gyne, ASUSIBR00000332); same as above, but 01 June 1995, 06:00 h (1 alate gyne and 1 male, ASUSIBR00000333-334); same as above, but 29 October 1995, 09:00 h (8 alate gynes and 8 males, ASUSIBR00000335-350); same as above, but 01 January 1996, 07:00 h (1 alate gyne, ASUSIBR00000351); same as above, but 10 February 1996, 07:00 h; col. Clayton R. R. Delabie (1 alate gyne, ASUSIBR00000352); same as above, but 20 February 1996, 08:00 h (1 alate gyne, ASUSIBR00000353); same as above, but 06 April 1996, 07:00 h (1 male, ASUSIBR00000354); same as above, but 14 July 1996 (5 alate gynes, ASUSIBR00000355-359); same as above, but 22 September 1996 (3 alate gynes, ASUSIBR00000360-362); same as above, but 26 October 1996 (2 alate gynes, ASUSIBR00000363-364).

Third collection site: BRAZIL, Bahia, Ilhéus, Praia do Malhado, from the drift line of the Atlantic Ocean on the beach; S14.781°, W039.045°; elevation above sea level: 0 m; collection date: 02 November 1994; col. Ivan C. do Nascimento (1 alate gyne, ASUSIBR00000065).

Description, paratype males Measurements (n = 25): TL 6.89–7.32, WL 2.25–2.47, HL 0.96–1.02, HW 1.00–1.07, IOD 1.25–1.33, ML 0.64–0.70, FLD 0.49–0.51, SL 1.31–1.45, EL 0.37–0.41, EW 0.38–0.43, PrW 1.23–1.44, FL 1.67–1.76, PL 0.37–0.44, PW 0.50–0.61, PPL 0.37–0.44, PPW 0.79–0.92, GL 2.15–2.47, CI 99–108, MI 64–71, SI 128-140. A small male (WL 2.25–2.47, TL 6.89–7.32), distinctly smaller than the male of the host species, A. rugosus . Integument smooth and shiny, thin, partly translucent. Body surface covered with few appressed, transversally flattened setae. Color uniformly pale yellow- to reddish-brown. Head Approximately as wide as long (CI 99–108); behind the level of the eyes, sides rounded and tapering towards the posterior margin of head; head size small relative to mesosoma . Mandibles long, slender, with distinct apical and preapical teeth, followed by seven to eight smaller, irregularly spaced teeth of irregular size; mandible surface smooth, shiny. Palp formula 4:2. Clypeus shape as in gyne; unpaired clypeal seta projecting over the anterior clypeal margin by two-thirds its length. Frontal lobes narrow, leaving the anterior half of the condylar bulbs exposed in full-face view. Preocular carina distinct, traversing the area of the antennal scrobe almost completely, nearly touching frontal carina. Eyes very large (EL 0.37–0.41, EW 0.38–0.43), strongly convex. Ocelli large, raised above the surface of the head; unpaired median ocellus approximately one and a half times wider than paired lateral ocelli. Antennae with 13 segments. Antennal scape long (SL 1.31–1.45) with appressed setae, surpassing the posterior margin of the head by half its length. Mesosoma Mesosoma with sex-specific modifications related to wing bearing. Anteriodorsal portion of pronotum inflated. Dorsolateral pronotal spine short, broadly triangular, and blunt in dorsal view. Ventrolateral pronotal spine absent. Dorsum of mesosoma smooth. Scutellum shape as in gyne; sculpture granulate with fine rugae. Bulla and meatus of metapleural gland small, orifice of metapleural gland tiny and round, pointing posteriorly, not notably modified from the condition in A. rugosus . Propodeal spines short, narrowly triangular, sharply pointed. Metasoma Petiole and postpetiole as in gyne. Gaster less bulbous than in host. First gastric tergite smooth, shiny, laterally with few reduced, rounded tubercles; sparsely covered with few appressed setae. Fore- and hindwings resemble the wings of its host, except for smaller size and a missing detached vein at the posterior end of the hindwing. Genitalia In toto, excluding the basal ring, parameres longer (1.04 mm) than wide (0.83 mm); apical lobe of paramere evenly rounded with less than 10 long, erect setae. In lateral view, aedeagus small (0.26 mm), ventral border of penis valve bearing 12 recurved teeth of uniform length; the anterior two and posteriormost of which are small and weakly sclerotized, whereas teeth 3-11 are distinctly larger and heavily sclerotized, as notable by the darker brown coloration.

Differential diagnosis The comparative morphological analysis reveals that A. fowleri is remarkably similar to its host species, A. rugosus ( Figs. 1 and 2 ). Notwithstanding, the gyne of A. fowleri can easily be distinguished from A. rugosus by the smaller size, the smooth and shiny integument, and the presence of appressed and transversally flattened setae ( Figs. 1 and 3b ). Relative to its smaller body size, A. fowleri is also characterized by longer appendages, and antennal scapes, as well as by a broader postpetiole ( Fig. 1 , Table 1). In the field, A. fowleri can be distinguished from its host by the significantly smaller size, the shiny appearance, the distinctly orange–brown coloration, the slowness of its movements, and the occurrence of alate females and males in some host nests throughout the year, whereas alates of A. rugosus typically occur during the rainier and warmer summer months (December–March) in coastal Bahia.

The male of A. fowleri resembles the male of A. rugosus and is not gynaecomorphic ( Fig. 2 ). Large males of A. fowleri reach the same size as small and medium size of A. rugosus males, but never reach the body size of large A. rugosus males. Despite slightly overlapping size ranges, the males of A. folweri can be distinguished from the A. rugosus males by their shiny integument, the slenderer and less bulbous gaster, the relatively longer antennal scapes, the absence of the inferior pronotal spine, the more pronounced tubercles on the first gastral tergite, and the presence of few, dorsoventrally flattened, appressed setae ( Fig. 2 , Table 1). The parasites’ genitalia are smaller than the hosts’ genitalia (paramere length: A. fowleri = 1.04 mm, A. rugosus = 1.66 mm), the length of the ventral aedeagal lobe is smaller in A. rugosus ( A. fowleri = 0.26 mm, A. rugosus = 0.21–0.22 mm; Fig. 4 ). It is important to note that the aedeagus of A. rugosus bears a very large dorsal lobe that is absent from A. fowleri ( Fig. 4 ). The ventral border of the aedeagus bears 12 teeth in A. fowleri and 12–14 teeth in A. rugosus ( Fig. 4 ).

Worker caste The worker caste is unknown and potentially nonexistent.

Etymology This inquiline social parasite is named in honor of our colleague, the late Harold Gordon Fowler, in recognition of his numerous important contributions to leaf-cutting ant biology, taxonomy, biogeography, and pest management in Brazil and Paraguay.

Previous studies referring to A. fowleri Acromyrmex fowleri was discovered 27 years ago and aspects of its biology were discussed in previous publications, where A. fowleri was referred to as either “ Pseudoatta new species”, “ Pseudoatta from Bahia ”, “ Pseudoatta from Brazil ”, or “ Acromyrmex new species” ( Delabie et al. 1993, Delabie et al. 2002; Schultz et al. 1998; Sumner et al. 2004; Schultz and Brady 2008; Rabeling and Bacci 2010; Soares et al. 2011; Rabeling et al. 2015). In this paper, we summarized the published and unpublished observations on the biology of A. fowleri . Key aspects of A. fowleri ’s biology and life history remain unknown and will require detailed field studies as well as conclusive behavioral experiments.

Figures

Fig. 1 Gynes of the social parasite Acromyrmex fowleri (a, c, e) and its host Acromyrmex rugosus (b, d, f) in full-face (a, b), lateral (c, d), and dorsal (e, f) views. The scale bars represent 0.5 mm in a and b, and 1 mm in c–f

Fig. 2 Males of the social parasite Acromyrmex fowleri (a, c, e) and its host Acromyrmex rugosus (b, d, f) in full-face (a, b), lateral (c, d), and dorsal (e, f) views. The scale bars represent 0.5 mm in a and b, and 1 mm in c–f

Fig. 3 Scanning electron micrographs of an Acromyrmex fowleri male (a) and female (b–f) depicting a the male head in frontal view, b the female head in lateral view, c the female maxilla showing the

Fig. 4 Comparative anatomy of male genitalia (a, b), female forewings (c, d), and female hindwings (e, f) of Acromyrmex fowleri (a, c, e) and Acromyrmex rugosus (b, d, f). The scale bars represent 0.1 mm in a, 0.2 mm in b, and 1 mm in c–f