Heteropodagrion Selys, 1885

Tennessen, Kenneth J., 2010, The madicolous nymph of Heteropodagrion sanguinipes Selys (Odonata: Megapodagrionidae), Zootaxa 2531, pp. 29-38 : 30-37

Heteropodagrion Selys, 1885

Description of final stadium nymph ( Figs. 1–12, 14 ). Stocky, compact body with short legs bearing numerous long hair-like setae and conspicuous patches of shorter, stout setae on dorsum of abdomen, and saccoid, setose caudal gills with filamentous tip ( Fig. 1).

Head. 1.90–2.05 times as wide as long, 1.13–1.17 times wider than widest point of synthorax (at mesepimeral processes above the mesocoxae). Postero-lateral lobes rounded, each bearing numerous small curved setae 0.04–0.10 mm long; dorsum of epicranium appearing granular; ventral carina of occiput near occipital foramen beset with numerous long pale setae that are aligned along lateral margins of withdrawn prementum. Antenna in life and in preserved specimens curved outward, then inward, as shown in fig.1; usually 7-segmented ( Fig. 2 ), rarely with 6 or 8 antennomeres; Antm1 nearly as long as Antm2; Antm2 only 1.2 times longer than wide, slightly longer than remaining antennomeres. Eyes large, in life light gray with darker mottling ( Fig. 14 ), in preserved specimens dark gray with slightly darker spots, ventro-lateral margins with a row of small, densely arranged, curved setae, below which are a few very fine, longer setae. Labium: articulation of pre- and post-mentum rests between bases of coxae I; prementum almost circular ( Fig. 3 ), lateral margins convex, ratio of length to maximum width 0.96–1.00; a long, slightly incurved row of very small transverse ridges on each side, tightly aligned; at high magnification, about 4 ridges per 0.1 mm ( Fig. 4 a), each ridge a simple raised area of the integument, varying from about 10 to 15 um high ( Fig. 4 b); no conspicuous dorsal premental setae (no raptorial setae is typical of Megapodagrionidae ) but with 8–12 fine setae visible in SEM photos; lateral margins of prementum without spinules, ventral surface scattered with long, hair-like setae slightly medial to lateral margin. Ligula convex, cleft, finely crenulated with a minuscule blade-shaped seta at the base of each notch between crenulations, and a small preapical tooth on each side of cleft ( Fig. 5 ). Labial palp without dorsal setae but ventral surface with a few fine hair-like setae pointing directly ventrally; distal margin below movable hook with 2 large processes and 1 smaller, rounded inner process ( Fig. 6 ); movable hook 0.77–0.88 times length of outer palpal margin. Mandibles with incisor and molar teeth ( Figs. 7 a, 7b), formula: L 1+2345 Oa(m1,2,3)b b' (1<3<2<5<4) / R 1+2345 y a b (1<3<2<4<5); 6–8 long curved setae at base on ectal surface.

Thorax. Prothorax with black, triangular epimeral processes extending laterally above coxae ( Fig. 1). Wing pads divergent, tips of hind wings reaching postero-laterally to posterior level of S6. Legs laterally depressed (width about 1.4 times thickness), mostly pale but patterned with gray blotches; femur short, apex not extending as far as tip of hind wing pad, and bearing long, hair-like setae and patches of stouter, shorter setae ( Fig. 8 ); tibia slightly longer than femur, patterned with gray blotches, bearing several patches of short stout setae, with numerous long hair-like setae on apical 2/3 and shorter, stouter and darker, slightly curved setae on distal 1/5; claw 0.18 mm long, 0.09 mm wide.

Abdomen. Cylindrical dorsally but flattened ventrally; patterned in dark markings shown in fig. 1, giving the appearance of a median pale stripe; S3–10 with dorsal tufts of curved setae forming an ill-defined setal row situated on dark markings on each side of median stripe ( Fig. 1). Lateral margins of S1–10 with numerous long hair-like setae; medial reddish markings on sometimes present on sternites S3–5 and S7–8. S3–8 with lateral slightly concave circular areas. Male cercus sub-rectangular with bluntly rounded apex ( Fig. 9 ), female cercus triangular ( Fig. 10 ). Male gonapophyses small, rounded, low tubercles; tips of female gonapophyses extending slightly beyond posterior margin of S10 ( Fig. 10 ), ventral margin of outer valves with numerous fine setae. S10 without dorso-medial excision. Caudal gills saccoid ( Figs. 1, 11 ) but with elongate depressions on each side of dorso-medial ridge and with ventral surface concave; gills slightly more than half length of abdomen, heavily setose, and with constriction (at about ¾ length) demarcating base of narrowly tapering, flexible apical filament ( Figs. 1, 11 ).

Measurements, H. sanguinipes : (males N=7, females N=4). Total length 8.75–11.5. Head length 1.67– 1.85, maximum width 3.40–3.60. Prementum length 1.90–1.94, maximum width 1.92–2.00. Hind femur length 2.55–2.70; hind tibia length 2.75–3.02. Abdomen length 3.8–6.5; cercus length 3 0.44–0.48, Ƥ 0.42– 0.43. Median caudal gill length 3.05–3.40; lateral caudal gill length 2.60–2.95.

F-1 measurements: Total length 7.15 – 7.40, head width 2.68–2.72, prementum length 1.52–1.54, prementum width 1.52–1.54, median gill 2.45, lateral gill 2.10–2.15.

Measurements, Heteropodagrion sp: (males N=1, females N=2). Total length 9.60–9.90. Head length 1.75–1.83, maximum width 3.50–3.65. Prementum length 1.94–2.01, maximum width 2.01–2.09. Hind femur length 2.70–2.85; hind tibia length 2.94–3.09. Abdomen length 4.4–4.9; cercus length 3 0.42–0.43, Ƥ 0.24– 0.32. Median caudal gill length 3.9–4.0; lateral caudal gill length 3.3–3.4.

F-1 measurements: Total length 7.2–8.3, head width 3.1–3.8, prementum length 1.62, prementum width 1.65, median gill 3.2–3.4, lateral gill 2.6–2.8.

Discussion and diagnosis. Heteropodagrion is in need of critical taxonomic study, as adults of H. sanguinipes appear to be variable in color pattern and morphology of the cerci (Garrison, pers. comm.). From the two described species, it has been suggested that Heteropodagrion superbum Ris could be a synonym of H. sanguinipes (Garrison et al. 2010) . It is possible that an additional taxon is involved in the samples I took, as adult males taken in Bolivar Province appear to be distinct from H. sanguinipes . Nymphs of the two populations are basically identical in general appearance and morphological details; however, I observed several differences: The molar crest of the right mandible of H. sanguinipes has teeth “a” and “b” equal in length, whereas in H. sp., tooth “a” is longer than tooth “b”. The movable hook in H. sanguinipes is 0.77–0.80 the length of the palpal lobe vs. 0.86–0.88 in H. sp. The hind femora of H. sanguinipes have only one distal patch of conspicuous stout setae on the dorsal carina vs. three or four in H. sp. Lateral gills varied in length from 2.58 mm to 2.95 mm in H. sanguinipes vs. 3.30 to 3.40 mm in H. sp. In H. sanguinipes, Antm 2 length was equal to or slightly greater than Antm1 length (ratio 1.00–1.04) vs. shorter than Antm1 (ratio 0.86–0.93) in H. sp.

Based on nymphs known to date, the genera of Neotropical Megapodagrionidae can be divided into two groups with the following character combinations:

Group 1). Antm1 relatively short (length less than half the distance between antennal bases), femora laterally compressed, S6–9 without dorsal hooks, and gills saccoid with a jointed, terminal filament [includes Dimeragrion ( De Marmels 1999; pers. comm.), Heteragrion ( Santos 1968, Novelo-Gutiérrez 1987, Ramírez 1992), Heteropodagrion , Hypolestes (Westfall & May 2000), Oxystigma ( De Marmels 1987) , Paraphlebia ( Novelo-Gutiérrez 2008) , Philogenia ( Ramírez-Ulate & Novelo-Gutiérrez 1994; Bybee & Tennessen 2008) and Sciotropis ( De Marmels 2004) ].

Group 2). Antm1 relatively long (length more than half the distance between antennal bases), femora not laterally compressed, S6–9 with dorsal hooks, and gills elongate, lacking a terminal filament [includes Teinopodagrion ( De Marmels 2001, von Ellenrieder 2006, Pérez-Gutiérrez 2007)]. Although the nymphs of Allopodagrion and Megapodagrion are unknown, they probably belong in Group 2 as they are related to Teinopodagrion based on adult characters ( De Marmels 2001).

Kalkman et al. (2010) termed Megapodagrionidae nymphs with saccoid gills “Balloon megapods” and listed all of the genera in Group 1 except two, Dimeragrion and Heteropodagrion , the latter unknown at the time of their publication. Dimeragrion was not included because the gills are nearly flat ( De Marmels 1999); the genus was therefore grouped with the “Fan megapods”. However, I believe that Dimeragrion belongs to the “Balloon megapods” because the gills have a terminal filament (not present in “Fan megapods”) and are slightly inflated with a thickened dorsal keel making them three dimensional.

Several characters separate nymphs of Heteropodagrion from the other genera in the first group (characters for Group 1 in parentheses): 1) prementum with a long, slightly curved row of small ridges on each side (without ridges); 2) ventral epicranial carinae near foramen (paralleling sides of prementum) with many long, hair-like setae (without setae or only one or two long setae); 3) Antm1–3 roughly equal in length (with either Antm2 and/or 3 at least twice as long as Antm1; exception Paraphlebia in which Antm2 is about 1.6 times as long as Antm1 and Antm3 is shorter than Antm1); 4) femora with small, isolated dorsal patches of two or more stout setae (without patches of stout setae); 5) hind femur short, when fully extended posteriorly apex is proximal to tip of hind wing pad of final stadium (extending beyond tip of hind wing pad). Heteropodagrion nymphs are most similar to Paraphlebia and Sciotropis , sharing the following traits: 1) antennomeres short and thick; 2) gills with many long, hair-like setae from base to apex; and 3) terminal filament relatively short and thick. In Paraphlebia , the prementum lacks the rows of small ridges, the dorsal carina of all femora have a singular row of short, stout setae, and the hind femora in the final instar extend beyond the tips of the hind wing pads ( Novelo-Gutiérrez 2008). Sciotropis is similar to Heteropodagrion in most characters, but the prementum is slightly longer than wide and lacks the rows of small ridges ( De Marmels 2004).

The tiny ridges on the prementum do not appear as highly effective aids for holding onto struggling prey. However, the ridges could increase friction and drag on prey when engaging small, segmented organisms, and because of the parallel, longitudinal orientation, could help direct the prey toward the mouth. Several small larvae of Chironomidae were found in the madicolous microhabitat. Because the nymphs must cling to the rocky surface, I would expect tarsal claws of madicolous nymphs to be short and stout, more so than in nymphs that occupy detritus or sediments in streams. This difference appears to be the case, as length by width ratios of Heteropodagrion and Paraphlebia zoe (also an inhabitant of vertical sheet flow, see Novelo- Gutiérrez 2008.) varied from 2.0 to 2.4, compared to ratios of 2.8 and 3.3 in Philogenia and Heteragrion which inhabit streams.

The generic description of the nymph of Heteropodagrion is based on two possibly distinct species. Adults of two possible new species are known to exist in Ecuador on the eastern side of the Andes (to be studied by J. J. Daigle, pers. comm.); discovery of the nymphs of these species is necessary to confirm or alter the generic characters proposed here.

Adult Heteropodagrion perch with wings closed in shade along small montane streams, usually near waterfalls. I am convinced nymphs do not inhabit the actual streams, as I have sampled these habitats for at least 100 man hours without finding Heteropodagrion nymphs. I finally found the nymphs by closely inspecting near-vertical boulders covered in sheet flow ( Fig. 13 ). Motionless nymphs were difficult to detect because their color pattern of yellowish orange and reddish brown blended with the background ( Fig. 14 ) resulting in remarkable protective coloration. Possible predators I saw in this habitat included spiders and beetle larvae, although there are undoubtedly others. The slightly concave and flattened underside of Heteropodagrion nymphs is an adaptation to these living conditions, designed for occupying sheet flow on high-gradient rock surfaces. The venter of the thorax is slightly concave, the abdominal venter is nearly flat, and the ventral surfaces of the lateral caudal gills are concave, all which undoubtedly aid the nymph in adhering to and maneuvering on the rock in the swift flow. I estimated the velocity of the water to be roughly 20 cm /sec. Despite the velocity, there is probably little drag on the nymphs due to frictional forces, as the water sheet itself tends to “cling” to the rock surface. I suspect that the contour and shape of the nymphs offers little in the way of resistance. The short, thick legs appear particularly strong. Disturbed nymphs ran or made herky-jerky movements in all directions on the vertical rock surfaces without losing their hold. When held in the palm of the hand and disturbed by a finger tip, nymphs would run and curl the tip of the abdomen up and forward over their dorsum (fig. 12); they appeared to poke the gills at the intruding finger tip. This behavior could be directed at an approaching predator; a detached hairy gill in the mouth of a predator might buy enough time for a Heteropodagrion nymph to escape.

At the locality where I found Heteropodagrion sp., I collected one nymph of Polythoridae that was clinging to the rock surface in open sheet flow within a few centimeters of several Heteropodagrion nymphs.

This nymph appears to be a species of Polythore , although I was unable to rear it and no adult Polythoridae were seen at this locality. The nymph is amazingly similar in overall appearance to Heteropodagrion , with compact tapering body, relatively short prementum (L/W = 1.12), angular projections on thoracic dorsum, setal patches on legs, and gills heavily setose with ventral surfaces concave. Despite its larger size and dorsal hooks, in dorsal view the resemblance of the polythorid nymph to that of Heteropodagrion is obvious. This might be a case of convergent evolution, in which a similar body style/shape evolved in distinctly separate lineages as a result of selective pressures imposed by a unique habitat. Novelo-Gutiérrez (2008) found similarities between nymphs of the megapodagrionid Paraphlebia zoe Selys and coenagrionids in the Argia extranea-vivida group, both inhabiting seepage habitats on rocky walls or nearby on the ground. I examined Argia nymphs from a vertical rocky seep near a waterfall in Cañar Province, Ecuador, which are probably Argia talamanca Calvert ; they have an overall appearance similar to Heteropodagrion , although they do not possess the angular projections on the dorsum of the thorax. Future research should be directed at the comparative morphology and behavior of various damselflies that occupy sheet flow and normal stream habitats.

Figures

FIGURE 13. Heteropodagrion sanguinipes. habitat of Heteropodagrion sanguinipes (photo by J. Johnson).

FIGURE 14. Live nymph of Heteropodagrion sanguinipes oriented head down on vertical rock face in sheet flow (photo by J. Johnson).

FIGURES 2 – 11. Heteropodagrion sanguinipes. 2) Right antenna; 3) Prementum, dorsal view; 4 a) ridges of prementum, dorsal view; 4 b) ridges of prementum at 45 ° angle; 5) Ligula; 6) Right palpal lobe; 7 a) Right mandible, ental view; 7 b) Left mandible, ental view; 8) Left hind femur; 9) Male cercus (c), lateral view (p = base of paraproct); 10) S 8 – 10, female, lateral view; 11) Left lateral gill, lateral view.