Ultrastructure of Wax-Producing Structures on the Integument of the Melaleuca Psyllid Boreioglycaspis melaleucae (Hemiptera: Psyllidae), with Honeydew Excretion Behavior in Males and Females

Abstract

The melaleuca psyllid, Boreioglycaspis melaleucae (Hemiptera: Psyllidae), was introduced to Florida as a biological control agent against Melaleuca quinquenervia, an invasive evergreen tree that has invaded large areas of Florida Everglades. Colonies of B. melaleucae nymphs are normally covered by white waxy secretions, and nymphs of various instars produce long bundles of white waxy filaments extending laterally and posteriorly from their abdomen. Scanning electron microscopy of 'naturally waxed' and 'dewaxed' nymphs (cleaned from wax) revealed two types of wax pore plates located dorsally and laterally on the integument of posterior abdominal segments starting with the 4th segment. Type-1 wax pore plates, with raised rim, peripheral groove, slits and pits, produce long ribbons and filaments of waxy secretions that are wound together forming long wax bundles, whereas type-2 wax pore plates, with slits only, produce shorter wax curls. Additionally, in both nymphs and adult females, the circumanal ring contained ornate rows of wax pores that produce wax filaments covering their honeydew excretions. Video recordings with stereomicroscopy showed that adult females produce whitish honeydew balls, powerfully propelled away from their body, probably to get these sticky excretions away from their eggs and newly hatched nymphs. Adult males, however, produce clear droplets of honeydew immediately behind them, simply by bending the posterior end of the abdomen downward. The possible role(s) of waxy secretions by nymphs and adults of B. melaleucae in reducing contamination of their colonies with honeydew, among other possibilities, are discussed.

Fig 1. Melaleuca psyllid colonies, eggs, nymphs, adults and waxy secretions.

A. White waxy secretions covering a colony of nymphs on a terminal shoot of melaleuca; ex, exuvia; unlabeled arrows indicate nymphs. B. Egg clusters, with their stalks embedded in leaf tissues. C. Nymphs of various instars with long wax bundles (arrows) extending laterally and posteriorly from their abdomens; inset shows an exuvia attached to the leaf with wax bundles still attached to it. D. Younger (2^nd instar) nymph producing a ball of honeydew (hd) covered with a thin layer of whitish waxy material. E. Older (4^th-5^th instar) nymph after ‘dewaxing’ (cleaning from wax by immersion in chloroform). F. Adult male (not dewaxed).

Fig 2. SEM of waxy secretions and wax pore plates on the integument of melaleuca psyllid nymphs (dorsal views).

A & B. Older (4^th-5^th instar) nymph with wax bundles (arrows) extending from the abdomen (ab); note that the head (h), thorax (th) and first 3 abdominal segments do not have wax bundles. C&D. Part of the abdomen in ‘dewaxed’ 4^th-5^th instar nymphs, showing arrays of wax pore plates of types 1 (p1) and 2 (p2), as well as the circumanal ring (cr) at the posterior end of the abdomen. E. Higher magnification of wax pore plates, types 1 (p1) and 2 (p2) in dewaxed nymphs; note the open slits (sl) in both types, and the pits (pi), peripheral groove (pg) and raised rim (ri) especially in type-1. F. Wax bundles (wb) coming out of type-1 pore plates (p1), and wax curls (wc) apparently coming out of type-2 pore plates (p2), on the abdomen of a waxed nymph. Additional abbreviations: cs, circumabdominal setae.

Fig 3. SEM of the circumanal ring, honeydew excretions and circumabdominal setae of melaleuca psyllid nymphs (dorsal views except in D).

A & B. Part of the circumanal ring (cr) around the anus (an) in dewaxed nymphs, with an outer row of wax pores (wp) and an inner row of slits (sl); ls, long setae; sp, rows of short spines pointed posteriorly. C. Circumabdominal setae (cs) covered with wax filaments in a ‘waxed’ nymph. D. Ventral view of the posterior end of the abdomen in a 2^nd-3^rd instar nymph with wax-covered honeydew (hd); cr, circumanal ring. E. Higher magnification of wax filaments covering honeydew excretions (hd) at the end of the abdomen; wb, wax bundles. Additional abbreviations: cs, circumabdominal setae.

Fig 4. SEM of adult females of the melaleuca psyllid at or near the posterior end of the abdomen.

A & B. Dorsal views of the circumanal ring (cr) around the anus (an) in a ‘dewaxed’ female, with the ovipositor (ov) and several long setae (ls) near the tip of the abdomen; note the divided-leaf like morphology of the circumanal ring (cr) and its double or multiple rows of wax pores (wp). C. Part of the abdomen’s end in a ‘waxed’ female, showing wax filaments (wf) oozing out of the circumanal ring (cr) and covering honeydew excretion (hd). D. Dorso-lateral view of the two ovipositor valvulae (ov), and details of their inner side (inset) showing several rows of fine ridges (arrow). E. Lateral part of the two abdominal terga anterior to the circumanal ring (cr) in a ‘dewaxed’ female showing type-2 wax pore plates (p2), with higher magnification in the inset; note multiple rows of short spines (sp) pointed posteriorly. F. Similar area to that in E, but in a ‘waxed’ female, showing type-2 wax pore plates (p2), with fine tufts of wax covering the terga and spines (sp).

Fig 5. SEM of adult males of the melaleuca psyllid at or near the posterior end of the abdomen.

A. Dorsal view of the anal tube (at), anus (an), aedeagus (ad) and two claspers (cl); the inset shows details of the anus (an), lacking a circumanal ring like that of the female (compare with Fig. 4A, 4B). B. Ventro-lateral view of the folded aedeagus (ad) and two claspers (cl); inset shows lateral view of tip of the anal tube (at) covered with thick hair, and several long spines (arrowhead) around the anus. C. Lateral part of an abdominal tergum anterior to the anal plate in a ‘dewaxed’ male showing type-2 pore plates (p2); sl, slits; sp, rows of short spines pointed posteriorly. D. Similar area to that in C, but in a ‘waxed’ male, showing type-2 pore plates (p2) and fine wax tufts covering the tergum and its spines.

Fig 6. SEM of the head and mouth parts of nymphs and adults of the melaleuca psyllid.

A. Ventral view of part of the head and mouth parts in a ‘dewaxed’ nymph, showing the clypeus (cl), two segments of the labium (lb1, lb2), extended part of the stylet bundle (es); retracted part of the stylets (rs) is looped behind the paired stylet-holding organ (so); inset shows nymphal antenna (at). B. Lateral view of terminal part of the stylet bundle, showing the (inner) maxillary stylets (mx), and serration (arrows) near the tip of the (outer) mandibular stylets (md1, md2). C. Ventro-lateral view of the head and mouth parts of an adult, showing the antenna (at), vertex (ve), compound eye (ce), two genal cones (gc) with long hairs/setae (arrowhead), partly extended stylets (st), and the labium (lb), between the two front coxae (co); upper and lower insets show details of distal segments of the antenna encircled with rows of short spines, with a long pointed bristle (arrowhead) at the end of the terminal segment.

Fig 7. Honeydew excretion behavior in melaleuca psyllid adults of both sexes.

A. Still image (taken from S1 Video), showing one female (fem, #4 in that video) with three excretion balls (eb1, eb2 and eb3) that were produced consecutively in the three clips shown in S1 Video (note the angle and distance between the female body and these 3 excretion balls). B. Melaleuca psyllid female at the beginning of the honeydew excretion process, with a tiny circle of waxy secretions (arrowheads in the inset) coming out of the openings of its circumanal ring (cr) near the posterior end of the abdomen. C&D. Still images taken from video, showing a male (in C) bending the posterior end of its abdomen downward to place a drop of honeydew (arrow) on the leaf surface, and the same male (in D) with several clear drops of honeydew excretions around it (arrowheads), with a larger drop (arrow) immediately behind its abdomen (note reflected light on each drop).