Nymphal and adult cephalic chaetotaxy of the Cydnidae ( Hemiptera : Heteroptera ) , and its adaptive , taxonomic and phylogenetic significance

Cephalic chaetotaxy of nymphal and adult stages of species from all the subfamilies of Cydnidae s. str. (sensu Froeschner, 1960 and Lis, 1994), namely Garsauriinae, Cephalocteinae, Cydninae, Sehirinae, and Amnestinae, was studied. Two types of setae, primary and secondary, are described, and changes they undergo during ontogeny reviewed. The adaptive, taxonomic and phyloge­ netic significance of the cephalic setae in the Cydnidae s. str. is discussed. A ground-plan of the original cephalic chaetotaxy of the family, and its evolution within the family Cydnidae s. str. are proposed.


INTRODUCTION
The presence of different types of setae on the body margins is typical of Cydnidae, a family of Pentatomoidea that includes many species living on and in the soil.Dif ferent types of setae (often stout, sometimes even peg-like or spine-like) are present on the margins of the head, tho rax, abdomen and always on the legs, particularly on the tibiae.Their function is still poorly understood, but are usually presumed to be tactile setae (mechanoreceptors) developed as an adaptation for burrowing (Froeschner, 1960;Dolling, 1981;Linnavuori, 1993).Signoret (1881) was the first to use characters related to the types, number and distribution of setae (mainly cephalic) for the classification of Cydnidae; he was fol lowed by Froeschner (1960), Dolling (1981), Linnavuori (1993) and Lis (1994).Moreover, certain characters con nected with cephalic chaetotaxy were regarded as of generic importance within the Cydnidae (Froeschner, 1960;Linnavuori, 1993;Lis, 1994).
Cephalic setae in adults of burrower-bugs are distrib uted mainly on the margins of the paraclypei, and some times also on the anterior margin of the clypeus; thoracic setae are present on the lateral margins of the pronotum, as well as on the corial margins of the hemelytra, whereas the abdominal setae are on the lateral margins of the sterna.Unfortunately, the chaetotaxy of the nymphal stages of Cydnidae is almost unknown; to date, nymphs (or their body parts) of all but a few species were described or figured (see Table 1) usually without refer ence to their chaetotaxy (Kobayashi, 1964;Lariviere, 1995;Linnavuori, 1993;Lis, 1992).
Although Cobben (1978) studied the cephalic chaetotaxy of nymphal and adult stages of numerous species from many heteropteran families, he concluded (op.cit., p. 61) that "there is no or hardly any ontogentic change in the cephalic sensory setae, but only phylogenetic disap pearance".However, during preliminary studies on the nymphal development of Cydnidae bred in the laboratory and preserved specimens, we noticed differences in the patterns of cephalic chaetotaxy of nymphal and adult stages.This was mentioned previously by Linnavuori (1993), who reported the loss of cephalic spines in adults of two species of Cydnidae, namely Geotomus hirtipes (Palisot de Beauvois) and Geocnethus pallipennis (Dallas).
The present study attempts to explain this phenomenon in Cydnidae, using more extensive material, and the value of cephalic chaetotaxy in the classification of the family.

MATERIAL AND METHODS
Material.This study was based on living specimens collected in Senegal by the second author, and reared in the laboratory, as well as preserved museum specimens from the collections of the Laboratoire d'Entomologie, Muséum National d'Histoire Naturelle, Paris, France (MNHN), and the Department of Bio systematics, Division of Zoology, University of Opole, Opole, Poland (DBUO).
List of species and stages studied (nymphal instars [N1 to N5] and adult [A]), and origin of specimens: Garsauriinae 1. Garsauria laosana J.A. Lis, 1991   Methods.The specimens were treated with KOH and depig mented in H2O2, if necessary prior to study.The heads were mounted in lactophenol or glycerol, and observed and drawn using standard optical equipment.
The concept of the family is that of Froeschner (1960) and Lis (1994); for a discussion of the composition of the family see Lis (1994, p. 7-9).

Primary setae
Cephalic primary setae (Fig. 1) appear to be a constant and basic character of nymphs and adults of almost all the species studied.
The general pattern of these setae is described for the subfamily Cydninae; for the other suprageneric groups of the family, modifications or exceptions to this pattern are given below.
Cydninae.The N1 of species of the subfamily Cydninae have six pairs of cephalic primary setae (Fig. 1); namely two setae (I-II) on the undersurface of an anterior part of each paraclypeus, three setae (III-IV-V) on the dorsal surface of each paraclypeus, and a single seta (VI) at the apical part of the eye.The same six pairs of setae (I-VI) are also present in N5 .Never theless, adults of a few species have fewer primary setae Sehirinae Sehirini.Only a single pair of primary cephalic setae is present in nymphal (N4-N5) and adult stages , namely the ocular apical seta (VI); this seta is sometimes very short and hardly visible, but is always present.All other primary setae are absent in the nymphal (N4-N5) and adult stages .Garsauriinae.The species of this subfamily have only four pairs of primary setae (III-IV-V-VI) in both nym phal (N5) and adult stages; setae I and II are absent (Fig. 26).The pairs III-IV-V are normally developed and obvious, although setae are usually torn out and thus may appear to be absent (therefore Froeschner, 1960, andDolling, 1981 recorded Garsauriinae as lacking cephalic setae).Setae III-VI in N5 of Garsauria laosana are pre sent in the same position as in N5 of all Cydninae (Fig. 26), but due to the allometric growth of the adult head the first paraclypeal pair of setae (III) is shifted anteriorly and thus directed forward (the same is true of adult G. aradoides Walker).The ocular apical seta (VI) in both N5 and adults of Garsauriinae is short, stout and sharp, and accompanied by a few additional stout sharp setae on the posterior eye margin.
Amnestinae.The number and arrangement of primary setae in the subfamily Amnestinae is very uncertain because only adults were studied.All six pairs (I-VI) of primary setae occur on the head (Fig. 27), although usu ally the apical eye seta (VI) is torn out and appears to be absent.The first pair (I) of primary setae is shifted for ward to the head margin or even onto its dorsal surface.Since sometimes there is an additional pair of paraclypeal setae on the dorsal margin of the head, adult Amnestinae appear to possess four to five paraclypeal primary setae (Froeschner, 1960).Nevertheless, the drawing of the 5th instar of a fossil Amnestus sp.(Thomas, 1988) indicates it has only three pairs of primary setae (III-IV-V), and thus  24,25) the fourth paraclypeal seta (regarded by Froeschner, 1960, as a primary seta) is an additional seta having nothing to do with the three primary setae.

Secondary setae
Cephalic secondary vestiture is only present in Amnestinae (Fig. 27), Cephalocteinae , and ; it is present in the first instar nymphs, at least in some species (Cydninae, Cephalocteinae).The secondary setae are absent in nymphs and adults of Garsauriinae (Fig. 26) and Sehirini .
These setae display a great diversity and are far more variable (in number, pattern and types) than the primary setae; moreover, they show a generic and intraspecific variation.
It was proposed previously (Lis, 1994), on the basis of their morphology, that the cephalic secondary setae can be classified into three groups as follows (already recog nized by Signoret, 1881).
There are, however, intermediate forms between types 1, 2 and 3, and it is sometimes difficult to ascribe a given seta to one of the three types.For instance, in genera Chilocoris Mayr and Amnestus Dallas it is difficult to decide whether the cephalic setae are of type (2) or (3) [setae on and close to the clypeus are very often "true-pegs", whereas those placed more posteriorly are "peg-like setae"].Therefore, for practical reasons two names -hair like setae [type (1)] and peg-like setae [types (2) and (3)] are suggested, as proposed by Froeschner (1960) and Lin navuori (1993).

Changes during ontogenesis
In all species whose nymphs were examined, the pattern of cephalic setae remains the same throughout nymphal life; the setae present in the first instar are present in the fifth instar nymph.
On the other hand, in some species, there are changes in the type and pattern of the setae in the adult stage.In a few species (Cydnus aterrimus, Endotylus brevicornis, Fromundus parcimonius, Fromundus glaber) the type of secondary setae appears to change during ontogenesis (peg-like setae in the 5th instar, hair-like setae in the adult - .But above all, there is a loss of setae in the adult stage.This is considered below by comparing the fifth instar nymphs and adult stages.

Comparison of nymphal (5th instar) and adult cephalic chaetotaxy
Depending on the species, there are some or no differ ences between nymphal and adult chaetotoxy.The differ- ences are mainly in the loss or regression of setae and can be divided into 9 categories (Table 2).

Adult and nymphal chaetotaxy differ
The cephalic chaetotaxy of adults differs from that of the nymphal stages; several kinds of modifications can be recognized within the Cydnidae regarding the loss of setae (primary or secondary) (Table 2); morphological modifications also occur.

DISCUSSION
The present study of the chaetotaxy of nymphal and adult stages of Cydnidae, in particular the changes that occur during ontogeny, provide information in three dif ferent fields: adaptation, taxonomy and phylogeny.

Cephalic setae an adaptive trait for a specific mode of life
The presence of cephalic primary setae, as well as two easily recognized types of secondary setae (hair-like and peg-like) in both nymphal and adult stages of Cydnidae, is unique to the Pentatomoidea; setae of similar stoutness and position are unknown in other shieldbugs (Dolling, 1981;Linnavuori, 1993;Lis, unpublished data).It is most probably connected with their mode of life -they live deep in the soil, under stones or in litter.Several facts or arguments support this hypothesis.
1.The development of tactile setae (mechanoreceptors) like primary setae is regarded by many authors (e. g., China, 1955;Cobben, 1978) as characteristic of all ground-living bugs; furthermore, among Pentatomomorpha this type of cephalic setae is known only in the Rhyparochromidae, which are also ground-dwelling bugs (Cobben, 1978;Schuh, 1975;Dolling, 1981;Henry, 1997).2. The rounded and usually flattened head of Cydnidae with its circular crown of setae (hair-like or peg-like) (Figs 28,32,34) suggests a bulldozer or a digger, well adapted for pushing and digging.Similar crowns of strong setae are found in the ground-dwelling nymphs of pentatomid species of the tribe Sciocorini, Menaccarus arenicola (Scholtz) (Putshkov, 1961;Lis, per sonal observation), as well as in the fossorial nymphs of Ochteridae [see in particular Dufour (1833), Bobb (1951) and Boulard & Coffin (1991)], a family belonging to the Nepomorpha.The crown of setae developed independently in the Ochteridae, which have the same mode of life, and cryptic behaviour.Moreover, nymphs in both families (Ochteridae and Cydnidae), construct cavities in which they rest or moult (Boulard & Coffin, 1991;Pluot-Sigwalt, unpubl.).Unlike Cydnidae and Menaccarus arenicola, adults of Ochteridae do not burrow and lack the crown of setae in the adult stage.3. Within the family, an absence of almost all cephalic setae (primary and secondary) is characteristic of the non-burrowing representatives of the Sehirinae Sehirini (all species live above ground, on plants).However, the nymphal and adult stages of species of Garsauriinae have three pairs of cephalic primary setae in spite of the fact that they are not fossorial, but live under the bark of trees.4. Unpublished observations on the biology and behav iour of several cydnid species seem to indicate a corre lation between the robustness of cephalic setae and the incidence of burrowing.All species with peg-like setae (Figs 32,33,34) probably burrow deeply (e.g., Chilocoris, Byrsinus, Stibaropus, Microporus), whereas those with hair-like setae inhabit the litter or live under stones (for instance Macroscytus brunneus -Fig.35). 5.A loss of setae in the adult stage may indicate a change in mode of life.Adults of many species are commonly collected on the ground or in a flight; they spend less time under ground than the nymphs.This was observed (unpubl.data) in Macroscytus brunneus, and probably in Endotylus brevicornis, Fromundus parcimonius and F. glaber.In the three latter species, the adults only have hair-like setae.Primary setae seem to be less obvi ously connected with fossorial habits than secondary setae, but setae I-II are only present in the soil dwelling Scaptocorini, Cydninae, and Amnestinae; they are absent in both the nymphs and adults of the above ground dwelling Sehirini and mycetophagous Garsauri inae.Moreover, setae I-II are absent in other represen tatives of Pentatomoidea (Lis, unpublished data).

Cephalic chaetotaxy as a taxonomic character
This study has confirmed that the head vestiture can have a taxonomic value.Congeners share the same type of cephalic vestiture, and undergo the same changes during ontogeny.However, there are exceptions, e. g., Macroscytus brunneus and M. australis, or Adrisa punctulata, A. similis, and A. rugosa, suggesting, most proba bly, the existence of species-groups within the genus.Moreover, as has already been noticed (Lis, 1994(Lis, , 2000)), the head vestiture differs between species and provides useful characters for their seperation.On the other hand, the taxonomic significance of the different types of sec ondary setae for defining the genera, should be re examined, because of the changes in vestiture that occur during ontogeny.It is clear that grouping species within certain genera solely on the basis of the cephalic vestiture is inappropriate, and must be supported by characters other than those associated with a specific mode of life.

Cephalic chaetotaxy as a phylogenetic criterion
As one might expect, the primary and secondary setae to be used in phylogenetic analyse; since each type of seta seems to have a different phylogenetic significance, they are discussed separately below.
Primary setae.The primary setae of the Cydnidae can be regarded as homologous to the cephalic setae of the nymphs and adults of many heteropteran groups (Leptopodomorpha; Gerromorpha; Ceratocombidae in Dipsocoromorpha; Plokiophilidae, Microphysidae, Anthocoridae, Nabidae, and Pachynomidae in Cimicomorpha; and Rhyparochromidae in Pentatomomorpha) and were consid ered by Cobben (1978), Schuh (1975), Dolling (1981), andHenry (1997) as trichobothria-like setae or true trichobothria.Moreover, the three pairs of trichobothria pre sent were regarded by China (1955), Cobben (1978) and Dolling (1981) as attributes possessed by the heteropteran ancestor, which (according to these authors) was a ground-living, hygrophilous bug.Thus, the occurrence of these three pairs of cephalic primary trichobothria-like setae (III-IV-V) in Cydnidae appears to be plesiomorphic, and a decrease in the number of these setae can be regarded as an apomorphy.The loss of the preocular pair of setae (V) occurs in some Geotomini (Adrisa rugosa and A. similis), and of all three pairs of trichobothria-like setae in all Sehirini.
The displacement of the three pairs of trichobothria-like setae (III-IV-V) in adults of Garsauria laosana and G. aradoides, along with the forward displacement of the first pair (III), can be considered a synapomorphy.
The absence of the apical ocular seta (VI) in nymphal and adult stages of Scaptocorini, as well as in adults of some Geotomini (Cydnochoerus nigrosignatus, Scoparipes affinis, all species of Adrisa), is also an apomorphic state.Since some Lygaeoidea (e. g., Rhyparochromidae) and many more primitive groups of Heteroptera possess two ocular setae (instead of one) in the early instars, the gradual disappearance of these setae in the Pentatomomorpha may indicate an anagenetic trend (see Cobben, 1978).
The primary setae I-II (on the undersurface of an ante rior part of each paraclypeus) were found only in Scapto corini, Cydninae and Amnestinae; they are absent in both nymphs and adults of Sehirini and Garsauriinae, as well as in other families of Pentatomoidea (Lis, unpublished data).Their presence can be regarded as a synapomorphy, and their absence in Sehirini and Garsauriinae should be most probably treated as a reversal homoplasious state.The displacement of the seta I and its movement up onto the dorsal surface of the paraclypei in Amnestus (Amnestinae) is an autapomorphy of the genus and of the subfamily as well.
Secondary setae.Based on the changes that occur during ontogeny we assume that the presence of peg-like setae in both nymphal and adult stages is the most archaic state in the Cydnidae.The following evolutionary changes can be regarded as apomorphies: (1) total reduc tion of the secondary setae in nymphs and adults -Garsauriinae and Sehirinae; (2) presence of peg-like setae in nymphs but absence in adults -Endotylus brevicornis, Fromundus glaber, F. parcimonius; (3) loss of the clypeal pair of secondary setae -Adrisa rugosa, A. similis, Endo tylus brevicornis, Fromundus glaber, F. parcimonius, Macroscytus brunneus, Aethoscytus multisetosus, Aethus lindbergi, Paraethus capicola); (4) fewer secondary setae in adults than in nymphs.
We conclude that the cephalic chaetotaxy of the Cydnidae-archetype included all the primary setae (I-VI), as well as a row of secondary peg-like setae along the entire lateral margins of the head (including clypeus) in both, nymphal and adult stages.Moreover, the three gen eral anagenetic trends in cephalic chaetotaxy in the fam ily Cydnidae can be hypothesized thus: (1) reduction in the number of primary setae, (2) reduction in the number of secondary setae leading in many cases to their entire loss, and (3) loss of peg-like setae during ontogeny.

Table 1 .
Literature on the chaetotaxy of the nymphs of Cydnidae -a summary.

Table 2 .
Main differences in the patterns of cephalic setae in Cydnidae [presence (+) and absence (-) of primary and secondary setae], and significant differences (loss of setae) between 5th instar nymph (N5) and adult (A) stages.++ in N5 and ++ in A = no change in number of secondary setae in adult compared to 5th instar; ++ in N5 and +-in A = decrease in number of secondary setae in adults compared to 5th instar.