Contributions to Zoology, 73 (4) 293-303 (2004)
SPB Academic Publishing bv, The Hague
the The shape of endemics: Notes on male and female genitalia in genus
Maniola (Schrank, 1801), (Lepidoptera, Nymphalidae, Satyrinae)
Andrea Grill Rob de Vos Jan van Arkel , , Institute for Biodiversity and Ecosystem Dynamics / Zoological Museum Amsterdam, University of
Amsterdam, P.O. Box 94766, NL-1090 GT Amsterdam, The Netherlands
Keywords:: Sardinian endemic, genital morphology, Maniola nurag
Abstract tion in genital morphology of the Meadow Brown
has been extensively discussed (Thomson, 1973,
for Butterflies of the genus Maniola are known their large 1976; Goulson, 1993). In recent decades, two new
at the inter- as well as intraspecific morphological variation, Maniola species have been described (Thomson, level. Given the overlap in wing-patterns, habitat selection, and 1987, 1990). First, the island endemic, Maniola chia geographic distribution of various Maniola species, genitalia Thomson, 1987, whose distribution is restricted to morphology is sometimes the only possibility to tell specimen Maniola hali- this describe characters the Greek island of Chios. Second, apart. In paper we diagnostic to distinguish Included Bo- different Maniola species by means oftheir genitalia. carnassus Thomson, 1990, which flies on the
is also the first detailed and illustration ofthe genitalia description drum peninsula (Turkey) and the Aegean island of
of the Sardinian endemic Maniola nurag. Further, apparatus Nissiros. Maniola endemic nurag(Ghiliani, 1852) is we describe two Sardinian individuals with intermediate char- and to Sardinia, a third endemic has been described Maniola and acteristics between nurag and Maniola jurtina,
discuss the from the island of Cyprus, Maniola cypricola propose that they are hybrids. Further, we shortly
justification ofthe species status for the island endemics Maniola (Graves, 1928) (for distribution areas of species
chia Maniola and cypricola. see Fig. 1). Maniola megala (Oberthiir, 1909) oc-
curs on the Greek island of Lesbos, throughout
southern Turkey and in Iran.
Contents Although neighbouring islands would be in flight
distance for all island endemics, the ranges of the
Introduction 293 island-Maniola species are well confined to the
Material and methods 296 borders of the respective island. In Chios, M. chia Dissection and photography 296 is said to entirely replace M. jurtina and Maniola Results 296
telmessia (Zeller, that are Discussion and conclusions 299 1847), species commonly
Acknowledgements 303 found on the neighbouring islands and the Turkish
References 303 mainland, which is only a few kilometers distant
from Chios. In the other M. Sardinia, on hand, nurag
flies sympatrically with M. jurtina. Although, the
Introduction latter species is usually concentrated on the coast,
whereas the Sardinian endemic has its distributional
“Made of and convex hills and val- up concave centres in the mountain areas of the island (> 500 of the first of the leys”, was one descriptions geni- m), there is a zone of overlap at intermediate alti-
tal of a male Meadow Maniola structure Brown, - tudes (500 900 m), where both species fly con-
meant to that this jurlina (L.), emphasize species’ temporarily at the same sites (Grill, 2003).
genitalia are irregularly shaped for a Satyrrd Butterflies of the Maniola known very genus are for Since varia- (Muschamp, 1915). then, geographic their large morphological variation (Fig. 2), at in-
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Fig. I. Distribution areas of the six European species of the
Maniola: Maniola M. genus (A) halicarnassus, (B) telmessia,
M. M. M. (C) nurag,,(D) chia, (E) cypricola, (F) M. jurtina.
both local ter- as well as intraspecific level, on and
continental scale (Ford, 1945; Thomson, 1973). 2. Variation in in the Maniola. the Fig. wing pattern genus All
Given the in selec- overlap wing-patterns, habitat specimens are in the collection of (he Zoological Museum
Amsterdam, Column shows the the tion, and geographic distributionofvarious Maniola Legend: (a) upperside, (b) underside of the butterflies: I. M. jurtina France (male), 2. M. species, genitalia morphology is sometimes the only jurtina France (female), 3, M. jurtina Sardinia (male), 4. M. tell What is possibility to specimens apart. more, jurtina Sardinia (female), 5. M. telmessia (male), 6. M. telmessia can also much within genitalia shapes vary a single 7. M. 8. M. intermediate (female), nurag (male), nurag form
the 9. M. 10. M. chia 11. M. chia species (Thomson, 1973). Nevertheless, spe- (male), nurag (female), (male),
12. M. 13. M. cies status of M. chia and M. cypricola has been (female), halicarnassus (male), halicarnassus (female), 14. M. cypricola (male), and 15. M. cypricola (female). justified mainly because of differences in the form
of the male genitalia; in wing-patterns they resemble
M. jurtina and M. telmessia, respectively. For the
third the underside endemic species in this genus,M. nurag, geni- wing markings.
talia structure and shape has never been described Ergo, the three main questions we address in this
in and illustrated detail as yet. paper are:
In this the of Are there characters in the paper, genital apparatus M. nurag 1) diagnostic genitalia
is described and illustrated in detail for the first of the different Maniola species?
time. We further describe two Sardinian individu- 2) What is the position of the Sardinian intermedi-
whose individuals in the Maniolal als, genitalia seem to be intermediates be- ate genus
M. and Is for M. chia and M. tween nurag M. jurtina. The genitalia mor- 3) species status justified
phology of these Sardinian specimens is compared cypricola?
the and of the in to shape structure genital organs
all M. other Maniola species, except megala, as this species can be unequivocally distinguished from
its congenerics by its appreciably larger size, and
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Material and methods Results
of In the main distinctive between In May 2002 we collected a series males and males, characters
females of M. 3 and M. Maniola are the of the the nurag (5 males, females) species shape valvae,
3 from Sardinia and the and size of the Julien jurtina (3 males, females) (Italy), gnathos, strength organ
in July 2002 M. jurtina (3 males, 3 females) from (Table 1, Fig. 3). There is also some variation in
Amsterdam (The Netherlands), and in September the aedeagus, but it is difficult to use this as a char-
of the same year M. chia (1 male, 3 females) from acter, as it has a rather soft structure and changes
Chios These its the from where (Greece). specimens were compared shape according to angle you
with specimens of M. telmessia (2 males, 2 females) look at it. The male genital apparatus also varies in
and M. halicarnassus (2 males, 2 females) collected size between species. Among the individuals we
in by H. van Oorschot in Turkey, present the Zoo- studied, M.jurtina has the largest and M. telmessia
the smallest found differ- logical Museum Amsterdam. Two of M. nurag the genitalia. In females, we
be attributed in of we dissected could not unequivocally ences the shape the ovipositor lobes and the
to M. to could of the ductus bursae In all nurag; according wing-pattern they length (Fig. 4). species
studied in this be a light, small M. jurtina as well as a dark large paper, except M. jurtina, the surface
of the bursa contains two that consist M. nurag. Small sample sizes are sufficient, as this copulatrix signa
of study aims at a qualitative and not quantitative spine-like sclerotised structures (Fig. 5).
description of characters. The butterflies were con-
served dry or frozen until preparation. Butterflies
were identified using characteristics in their wing- Maniolajurtina (Figs. 3A, 4A)
patterns following Hesselbarth et al. (1995), van
Oorschot & van den Brink (1992) and Tolman & Male: Gnathos markedly swollen at the base, then
Lewington (1997). All individuals studied are in quickly narrowing. Valvae bigger than all other
Amster- the collection of the Zoological Museum, species except M. halicarnassus, in shape most
dam. similar M. but with characteristic to nurag, a curve
towards the distal distal and dorsal process; pro-
cess round; ventral edge different from the other
Dissection similar Julien and photography Maniola species, most to M. nurag.
thick and organ always clearly visible, very strong,
of Prior to dissection the abdomen the specimen can be twice the size as in congenerics.
Female: was separated from the rest of the animal and soaked Length of ductus bursae comparable to
in Potassium hydroxide (KOH 10%) for approxi- the other species; notably in none of the dissected
mately 15 hours. To stabilize the samples for pho- females we found signa, although they were clearly
in visible all female individuals the tography, they were positioned laterally a small in of other spe-
drop ofethanol (30%), flattened between two glass cies. The absence of these marks might be a good
M. and lids. They were photographed under the microsdppe distinctive characteristic between jurtina in (magnification x 25). In order to photograph the the other species the genus Maniola.
form of the signa in the bursa copulatrix, which
distinctive characteristics may show important
between species, the female genitalia were dyed Maniola telmessia (Figs. 3B, 4B)
with chlorazolblack. The dye was fixed in 95%
For in ethanol. handling, the genitalia were kept Male: Genital apparatus clearly smaller than in all
30% ethanol, as in stronger concentrations of etha- other Maniola. Gnathos similar to M. chia, slightly
nol the chitine hardens and breaks easily. For long swollen at the base, vesica round. Valvae similar
term conservation the genitalia will be transferred in shape to M. chia and M. halicarnassus; distal
to a or slide. similar to M. chia and M. glycerol-tube Euparol process pointed, nurag,
dorsal process almost pointed. Ventral edge simi-
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telmessia considerably pointed flatflat jurtinajurtina to othersothers inin cypricola gradually inin telmessia all continues thanthan in base, in curves M. rounded, than at comparable pointed than flat, than fragile swollen narrowingnarrowing small, sizesize sharply longer clearly begins stronger inin angle, more
pointed in gradually jurtina thanthan to not but stronger halicamassushalicarnassus rounded, base, comparable but M. at size thick narrowingnarrowing large, sharplysharply pointed curvedcurved fragile, telmessia in
off Maniola Maniola base.base, . broken other telmessia at other other in all often genitalia. M. swollen than than M.telmessia fragile, male slightly smaller smaller pointedpointed pointed curved i veryvery
the size of in jurtina pointed flat base.base, basis thanthan in chiachia at nurag telmessia, jurtina the continuescontinues in to curves M. in flatterflatter jurtina on swollen than than flat, toto andand than so comparable species slightly less larger widewide pointed begins angle, similar
Maniola ,, jurtina jurtina gradually jurtina curved inin telmessia telmessia than nurag in in than than M.nurag base, in than M. than thanthan at than flatter pointed differentiate than flat, fragile swollen narrowingnarrowing smaller larger round, clearly begins more stronger to
base, Maniola characters curve at processprocess curved narrowing other of jurtinajurtina than swollen all strong M. dorsal than characteristic flat, listing quicklyquickly and markedly thenthen larger with towards round round begins thick Comparative process process edge organorgan 1. character Table gnathos valvae dorsaldorsal distal ventral Julien
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3. Male of different Maniola M. M. telmessia, M. M. M. Fig. genital apparatus species. (A) jurtina, (B) (C) nurag, (D) chia, (E)
halicarnassus, (F) M. cypricola, and (G) intermediate form (from Sardinia).
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lar to M. chia and M. differ- halicarnassus, clearly cess pointed, dorsal process sharply rounded but
ent from Julien M. jurtina. organ present but very not pointed, connection between distal and dorsal
In M. telmessia the Julien often brakes than fragile. organ process straighter in other species. Ventral edge and in earlier off, literature it was considered to be similar to M. telmessia. Julien organ thinner than references in lacking (see Thomson, in M. M. and but 1973). jurtina, nurag M. chia, stronger Female: Ductus bursae similar to M. nurag and than in M. telmessia.
M. chia; signa clearly visible, short, pointed at the Female: Ductus bursae slightly longer than in
posterior end, broadening at the anterior end (Fig. the other species; signa variable, but clearly vis- 5A). ible, pointed towards the posterior end, broaden-
ing towards the anterior end (Fig. 4D).
Maniola nurag (Figs. 3C, 4C)
Maniola cypricola (Fig. 3F)
Male: Gnathos substantially swollen at the base,
vesica round its Valvae at extremity. considerably Male: swollen Gnathos at base, gradually narrow- smaller than in M. jurtina but larger than in M. ing. Valvae small, comparable to M. telmessia in telmessia. Dorsal visible, process clearly round, size and line towards distal shape, process straight, flatter than in M. jurtina: distal process clearly as opposed to all other species, where it is slightly pointed, sharper than in M. jurtina: ventral edge distal dorsal curved; process clearly pointed, pro- similar curved, to M. jurtina. Julien organ present, cess sharply rounded, basis considerably longer than more fragile than in M. jurtina, but stronger than in other Maniola. in M. telmessia. Female: Ductus bursae relatively short; signa Female: Ductus bursae similar to other Maniola clearly visible, elongated, round at the ends (Fig. species; Bursa with two elongated signa, which vary 4E). considerably in length and visibility (Fig. 5B).
Intermediateform (Fig. 3G) Maniola chia (Figs. 3D, 4D)
The two individuals with wing-patterns that seemed Male: Gnathos slightly swollen at the base, but less intermediates between M. and M. nurag jurtina, than in M. nurag, shape and size of aedeagus simi- were also intermediate in genitalia structure. lar to M. nurag. Valvae larger than in M. telmessia, Male; Gnathos markedly swollen at base, then comparable to those ofjurtina in size, but not in Valvae than in M. quickly narrowing. larger nurag; shape; distal pointed similar to M. telmessia process distal like in M. but process pointed nurag, posi- and M. dorsal wider and flatter than nurag, process tion like in M. dorsal jurtina, process slightly pointed in M. and Ven- jurtina M. nurag, slightly pointed. as opposed to the other two species; ventral edge tral edge differently curved thanin M. jurtina, similar similar to M. Juhen jurtina. organ thicker, but not M. telmessia. Julien like to organ in M. jurtina. as solid as in M. jurtina. Female: Ductus bursae relatively short, notably We able were not to identify any females of this shorter than in M. halicarnassus; Bursa in all indi- type. viduals with two crescent-formed signa (Fig. 5C).
Discussion and conclusions Maniola halicarnassus (Figs. 3E, 4E)
(1) Are there diagnostic characters in the genitalia Male: Gnathos thicker at the base but gradually of the different Maniola species? narrowing towards the end. Valvae of similar size In females, the most unequivocal characteristic as in M. but different in jurtina, shape; distal pro- to M. from the other five distinguish jurtina spe-
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4. Female of different Maniola in M. M. M. Fig. genitalapparatus species comparison. (A) M. jurtina, (B) telmessia, (C) nurag, (D)
chia, (E) M. halicarnassus, and (F) M. cypricola.
of this cies we studied, seems the absence signa on the ally to genitalia structure, differentiate species
all studied in- from Maniola. of female bursa. Signa were present in the other More a problem poses
which is similar dividuals M. nurag, M. chia, M. cypricola, M. tel- M. chia, very to M. telmessia in
messia, and M. halicarnassus, but absent in M. the shape of its genital apparatus, and almost in- jurtina. However, it might be, that this character- distinguishable from M.jurtina by its wings. Maybe
istic is just much rarer in M. jurtina than in the it is this intermediate position between M. telmessia
other species, but still occasionally present (Thom- and M. jurtina, that can serve as a distinctive charac-
The female ofthe other teristic: chia = like telmessia son, pers. comm.). genitalia genitalia plus wing-
Maniola species do not show diagnostic charac- pattern of jurtina. But obviously, for this species
As main characters ters. usual, the to differentikte more samples are necessary to obtain a better pic-
between species are in the male genital apparatus. ture.
be Maniola jurtina can clearly distinguished by Thomson (1973) divides the species M. jurtina
shape and size of the valvae and the Julien organ. into three main types, the eastern, the western, and
Maniola is well the where in the the nurag generally recognisable by primitive type, primitive type
has the form of its valvae. Maniola telmessia is dis- dorsal process an irregular ‘fringe’, which usu-
outline of the val- extends the distal in the tinctive by its smaller size, the ally to process, western
of distal and dorsal the dorsal is with vae and the shape processes. In type process long a pointed or
M. halicarnassus the form of the dorsal process as very sharply rounded extremity or a short flat top,
in the well as the connection between dorsal and distal and eastern type the dorsal process is fairly
distinctive. is further facili- short with flat almost flat Also process are Diagnosis a or top. the gnathos
tated the which addition- and the ventral the three through wing-patterns, edge vary among types.
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5. in the bursa M. M. M. M. M. Fig. Signa female copulatrix of (A) telmessia, (B) nurag, (C) chia, (D) halicarnassos, and (E)
cypricola.
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the ofM. What is the of the Sardinian interme- He postulated that genital apparatus nurag (2) position
individuals in the and M. telmessia were close to the western type he diate genus Maniola? individuals with intermediate found in M. jurtina. At the time his publication In the two Sardinian
also the intermediate appeared, M. halicarnassus and M. chia were not wing-patterns genitalia are of
in their resemble M. described yet, and consequently he could not dis- form; contours they jurtina,
but are smaller and the distal is cuss them at the time. According to his ideas, the they process pointed
individuals in the eastern of like in M. and M. telmessia. The explana- primitive type range nurag
relict tions for this are twofold: (1) These two individu- M. jurtina are elements of the original type
als are between M. and M. of Maniola, which were the ancestors ofall Maniola hybrids jurtina nurag,
and therefore have intermediate wings as well as species we know in Europe today. He found the
genital structure. (II) There is a third form of Maniola eastern forms with the primitive valvae in moun- in Sardinia. This intermediate type, however, tain localities from 1500 - 2000 metres a.s.l., and flying is similar clearly more to M. nurag and M. jurtina, concluded that the Iranian forms of M. jurtina are than of the other Maniola which the oldest of this to any species, probably surviving ancestors ge- makes the hybrid-idea plausible. Considering the nus, which he considers originally a mountain spe- similarities in size and structure of the genitalia in cies. From Iran, he suggests, the butterflies have M. jurtina and M. nurag, hybridisation seems theo- travelled westwards in two flows, one towards the The ‘intermediate’ form Differen- retically possible. new we south, the other one towards the north. found in Sardinia is another for the po- tiation of the southern resulted in example, migrant groups of the tential genus Maniola as an interesting model what he calls the western type of valvae, and the and system to study adaptation speciation processes. northern migrants led to the eastern type. M. telmes- sia would be the result of an extreme differentia- (3) Is species status justified for M. chia and M. tion of the western type, that had become so differ- cypricola? ent from the ancestors that it resisted a reinvasion Considering the intraspecific variation in the male of the eastern type M. jurtina later on in the areas genital apparatus, illustrated by Thomson (1973), of what we call Greece and Turkey today, which is from different in the in M. jurtina areas Europe, in why we find M. telmessia and M. jurtina flying use of genitalia structure to justify species status sympatry in most of their ranges. Thomson (1973) remains problematic. The characters we give in Table further that M. is the furthest de- suggests nurag 1 provide guidelines for differentiation between velopment of the M.jurtina ancestor. He bases this different Maniola species, but have to be used in on the fact that the valvae are purely of western combinationwith wing characteristics and ecological form, and the fulvous of the butterfly is very ex- data of the site where the specimen was collected. tensive. Although all this reasoning is very intrigu- The wing-patterns of M. chia, forexample, resemble ing, and indeed partly convincing, it remains in the those of M. jurtina (Fig. 2) so closely, that these realm of conjecture. To answer questions like that, two species are indistinguishable without taking into large scale phylogenetic and phylogeographic analy- account the geographic provenance and male geni- sis based on molecular data are indispensable. talia structure of the specimen. Also M. cypricola The illustrations presented in figure 3 show that is phenotypically extremely similar to M. telmessia. the six based on male genitalia shape, species we On basis of the valvae, however, M. chia and M. M. telmes- investigated would fall into two groups; cypricola can be clearly distinguished from the other sia, M. M. M. on the halicarnassus, chia, cypricola Maniola. What is that more, given these two spe- and and the other. one hand, M. nurag M.jurtina on cies are island endemics and therefore completely This pattern corresponds well to the geographic isolated from other congeneric populations, they distribution of these the first four are species: fly- In are a genetically distinct entity. a nature conser- ing in the eastern Mediterranean, the latter two in vation context they would therefore be considered also confirms the western Mediterranean. It our if as ‘evolutionary significant units’, regardless they M. genetic data on the close genetic relationship of are ‘real’ endemic species or not (Gardenfors et and M. (Grill, 2001; Grill, 2003). nurag jurtina al., 1999).
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Acknowledgments Grill A. 2003. Endemism in Sardinia: evolution, ecology
and conservation in the Maniola PhD butterfly nurag.
thesis. University of Amsterdam. We cordially thank Harry van Oorschot for his kind advice.
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