Journal of Threatened Taxa |
www.threatenedtaxa.org | 26 February 2021 | 13(2): 17722–17730
ISSN 0974-7907 (Online) | ISSN 0974-7893
(Print)
https://doi.org/10.11609/jott.6656.13.2.17722-17730
#6656 | Received 09 September 2020 | Final
received 16 November 2020 | Finally accepted 27 January 2021
First
record of the early immature
stages of the White Four-ring
Ypthima ceylonica (Insecta: Lepidoptera: Nymphalidae), and a note on a new host plant from India
Hari Theivaprakasham 1, Hari Ramanasaran 2 & Appavu Pavendhan 3
1 2 3 The Nature and Butterfly Society
(TNBS), 8, AKG Nagar, 3rd Street, Uppilipalayam,
Coimbatore, Tamil Nadu 641015, India.
1 theivaprakasham@gmail.com
(corresponding author), 2 ramanasaran21@gmail.com, 3
appavu.pavendhan@gmail.com
Editor: B.A. Daniel, Zoo
Outreach Organisation, Coimbatore, India. Date
of publication: 26 February 2021 (online & print)
Citation: Theivaprakasham,
H., H. Ramanasaran & A. Pavendhan
(2021). First
record of the early immature stages of the White Four-ring
Ypthima ceylonica (Insecta: Lepidoptera:
Nymphalidae), and a note on a new host plant from India.
Journal of Threatened Taxa 13(2): 17722–17730. https://doi.org/10.11609/jott.6656.13.2.17722-17730
Copyright: © Theivaprakasham
et al. 2021. Creative Commons Attribution
4.0 International License. JoTT allows unrestricted use, reproduction, and
distribution of this article in any medium by providing adequate credit to the
author(s) and the source of publication.
Funding: This research did
not receive any specific grant
from funding agencies in the public,
commercial, or not-for-profit sectors. All visits and
work were self-funded.
Competing interests: The authors
declare no competing interests.
Author details: H. Theivaprakasham is a Coimbatore-based naturalist and Co-founder of The Nature and
Butterfly Society (TNBS). He is an engineering graduate from Amrita School of
Engineering, Coimbatore. He has been researching butterflies of the Western
Ghats for nearly a decade. He specializes in the immature life stages of
butterflies. H. Ramanasaran from Coimbatore, Tamil Nadu is one of
the Executive Members of The Nature and Butterfly Society (TNBS). He is a
pharmacy graduate who is actively involved in observing and documenting the
birds and butterflies in and around Tamil Nadu and Kerala for the past 8 years.
He also observes the primary stages of the butterflies. Appavu Pavendhan from Coimbatore, Tamil Nadu is the
President of The Nature and Butterfly Society (TNBS). He is a postgraduate in
textile engineering from Anna University, Chennai, and has over 30 years of
professional experience including serving as a scientific officer in a Research
Association. His interest in nature includes birds and butterflies among others
and has been keenly observing them for the past 10 years.
Author contribution: HT—involved in field sampling,
data analysis and manuscript drafting. HR—involved in field sampling, data
collection, data supervision and manuscript editing. AP—involved in data
analysis, data validation and manuscript editing.
Acknowledgements: We are
grateful to Mr. Keith V.
Wolfe (California, USA)
for his comments and improvements of
this manuscript. We
would also like to thank the entire
executive team of TNBS including Mr. Nishanth C.V., Mr. Viswanathan S., Mr. Gopalakrishnan S., and Mr.
Balakrishnan R. for accompanying us during
field trips in search of the larva and host
plant.
Abstract: Documentation of the early immature stages (egg, larva, chrysalis) of the White Four-ring (Ypthima ceylonica Hewitson, 1865), including
larval morphology and behaviour, is described for the first time from India. A new host plant (Cynodon dactylon (L.)
Pers.) is also reported
for this butterfly.
Keywords: Cynodon dactylon, juvenile
biology, life history, Poaceae, Western Ghats.
Introduction
The genus Ypthima under
the family Nymphalidae (Satyrinae)
was first described by Hübner in 1818. These butterflies have dull to dark brown
wings with a large ocellus on the forewing and a series of submarginal
ocelli on the hindwing. Currently, Ypthima includes nearly 113 species
widespread across the southeastern fringe of the
Palearctic Region, Afrotropical Region, and Oriental Region (Shima & Nakanishi 2007). In India, 35 species are known to occur
(Varshney & Smetacek 2015).
The White Four-ring Ypthima
ceylonica, is an uncommon butterfly
distributed over the southern Indian states (Andhra Pradesh, Karnataka, Kerala, Tamil Nadu, and Telangana), a West
Indian state (Maharashtra), East Indian states (Odisha and West Bengal) and
several regions of Sri Lanka. The
species was first described from Sri Lanka in 1865 by Hewitson. Moore (1880) recorded the species from Gale
and Colombo, Sri Lanka. In India,
Marshall & de Nicéville (1882) recorded that the
species was distributed across southern India starting from Travancore and
Madras to Odisha and a similar observation was made by Moore (1893). Hampson (1888) recorded the species from the Nilgiris Hills.
Bingham (1905) extended the distribution to Bengal and also considered Y.
ceylonica as a race of Ypthima
huebneri Kirby, 1871, rather than treating them
as separate species. However, the male genitalia has been shown to provide
important information for the identification of Y. ceylonica (Elwes &
Edwards, 1893). The recent study by
Chandra et al. (2007) has expanded this species’ range to the states of Madhya
Pradesh and Chhattisgarh.
The first incomplete observation of Y. ceylonica’s early stages was made from Sri Lanka in 1910 by Green. This was
followed by a detailed description and colour images by van der Poorten & van der Poorten
(2012). Though there are two detailed
descriptions of the immature stages of Y. ceylonica
from Sri Lanka, to the best of our knowledge and after extensive literature
review, there is no documentation on the early immature stages from India. Thus, we take this opportunity to describe
the various instars and report a new larval
host plant for Y. ceylonica.
Materials
and Methods
A female Y. ceylonica was found ovipositing
on two grass species, Cynodon dactylon and Axonopus
compressus (Sw.) P.Beauv. One egg and plant material were collected
from the first author’s garden (11.030N, 76.902E) located at Coimbatore, Tamil
Nadu, India. The collected egg and plant
material were placed in a plastic rearing container. The various stages of egg, larva, chrysalis
and adult were photographed using a Sony HX60V digital camera. The size of the egg was measured using the Digimizer image analysis software, and the size of the
larva and chrysalis were measured using a standard measuring scale. The excreta of the larva was removed and the
container was cleaned daily to prevent microbial infection. The larva was supplied with fresh leaves of
its host plant, C. dactylon, whenever
required. The described larval segments
and morphology are based upon the annotated image shown in Image 1.
Results
Egg
The adult female laid eggs on the underside of both
green and dry leaf blades of C. dactylon
and A. compressus very close to the
ground. The female was also observed to
lay eggs on such nearby objects as a plant’s dry leaf, branches, sticks and a
stem found in close proximity to the host plant (Image 2). The collected egg measured 0.75mm at its
longest diameter. The egg was dull white,
almost globular with a nearly flat base and top, and the surface had many small
irregular polygonal facets (Image 3a–f).
The egg started to develop dark pink striations on day 4 (Image 3d) that
continued till the egg matured on day 6 (Image 3f).
First instar
At the end of day 6 (Image 4a), the neonate larva
enclosed by nibbling a portion of the egg.
The hatchling completely consumed the eggshell as its first meal. The first-instar larva was cylindrical and
measured 2.5mm in length. The head was
pale brownish pink and covered with numerous setae. The body was pale pink with a dark pink
mid-dorsal band bordered with thin white bands.
The sub-dorsal band was thin, dark pink and bordered with thin white
bands. The broad spiracular band was
pink and bordered with a thin dark white band.
The thin sub-spiracular band was pink.
All dorsal and ventral bands ran longitudinally from the head to the
anal segment. Numerous setae arose from
the tubercles on its body. The larva had
a pair of short projecting conical horns on the dorsolateral portion of its
head and a pair of pointed conical anal processes. On day 8 (Image 4b), the larva fed on young
tender grass blades and started to acquire its pale green undertone, which
increased day by day (Image 4a–f). The
broad pink spiracular band also started to become progressively thinner. After 14 days (Image 4f), the larva moulted
and the body length increased to a maximum of 3.2mm.
Second instar
In the second instar (Image 5a–j), the body was dull
white initially, with the larva acquiring a green undertone over the next few
days (Image 5f–j). The sub-spiracular and spiracular bands became darker, while
the mid-dorsal band turned dark green and the sub-spiracular band turned
white. The head, which was dark pinkish
at the end of the first instar, started to lighten. The length of the body setae gradually
decreased in size, while the anal processes became darker, and grew thicker,
longer and more pointed. The
second-instar larva was more active at night than during the day. Whenever disturbed, the larva, which
preferred to eat fresh grass, instantly dropped from the leaf to the bottom of
the container. The second instar lasted
for eight days. The body length
increased from 3.2mm to 5.2mm starting from day 14 (Image 5a) until day 22
(Image 5j).
Third instar
The third-instar larva (Image 6a–n) was light brownish
in colour on day 23 (Image 6a), turning pale greenish on day 24 (Image
6b). The setae were drastically reduced
in size compared to the second instar.
The body was pale green with a dark green mid-dorsal band, and the
spiracular band was bordered by a thin white line. The sub-dorsal band was thin, dark green and
bordered with thin alternating white and dark green lines that ran
longitudinally from the head to the anal segment. The conical anal processes were pale pink,
the head turned pale green from its earlier pale brown colour and the
sub-spiracular band was white. Starting
with day 30 (Image 6g), the upper border of the sub-spiracular line developed
thin brown markings. The third instar
lasted about 14 days with the body length increasing from 5.2mm to 13mm. The larva moulted on day 38.
Fourth (final) instar
The fourth-instar larva (Image 7a–j) was different
compared to the third instar. The body
was pale brown and the mid-dorsal band was dark brown with thin white
borders. The broad dark brown spiracular
band was bordered with thin white lines, and a white line was observed running
close above the spiracles. The
sub-spiracular band remained white. The spiracles
were black and became more prominent compared to earlier instars, while the
head and the anal processes were pale brown.
The larva fed voraciously on the host plant grass, usually choosing a
long blade and feeding from the tip to its base. The larva was observed to reach a leaf’s
topmost part to feed during the night and return to the bottommost part by
morning. It was also observed to rest
lengthwise on half-eaten blades. The
interesting behaviour of forceful frass ejection was
also noted, which is best known in species of shelter-building Hesperiidae, but also witnessed with larvae in the Papilionidae, Pieridae, Nymphalidae and numerous moth families (K. Wolfe, pers.
comm.). Besides Indian Y. ceylonica and Ypthima
striata Hampson, 1889 (TH, pers. obs.), this
likely predator-distancing strategy is practiced elsewhere by Ypthima huebneri (Tan,
2015), Ypthima pandocus
corticaria Butler, 1879, and Ypthima
baldus newboldi
Distant, 1882 (Tan 2014a,b). The fourth
instar lasted for eight days, and on day 45 (Image 7i), the body length
increased from 13mm to a maximum of 18mm.
After day 44, the larva stopped feeding on the leaves and started
searching for a suitable place to pupate.
The larva chose a blade of grass on which to pupate and gradually reduced
its body length to 8mm. The larva
remained stationary and pupated on day 46 (Image 7j), the pensile chrysalis
being attached by its cremaster to a silken pad spun
by the larva.
Chrysalis
The chrysalis (Image 8) was dull yellow, covered with
brown striations and measured 10mm. The
general profile was elongated and convex except for a conspicuous bump near the
junction of the thorax and abdomen. The
ocular caps were pointed and short while the wing cases were bordered with a
brown line. The chrysalis turned increasingly darker each day. On day 53, the pupal case became transparent
and the subapical ocelli marking of the pharate butterfly became visible. On day 54, an adult female emerged in the
early morning and was seen resting upside down, drying its wings and ejecting
red meconium fluid. Overall, the
chrysalis stage lasted for nine days.
The total growth period from egg to adult spanned 54
days, with the development of egg (six
days), first instar (eight days), second instar
(eight days), third instar (14 days), fourth instar (nine days) and
chrysalis (nine days).
Discussion
Our observations in this study in India had various
striking differences in host plant selection, larval and chrysalis stages when
compared with the earlier descriptions (Green 1910; van der Poorten
& van der Poorten 2012) from Sri Lanka. The following discussion focuses on
comparisons with those earlier studies.
Host plant
Various grass host plants for Ypthima
ceylonica are reported from Sri Lanka and India,
all from Poaceae.
In Sri Lanka, Green (1910) reported Phalaris
arundinacea L. and van der Poorten
& van der Poorten (2012) reported Axonopus compressus
and Cyrtococcum trigonum
(Retz.) A.Camus as host plants. In India, Nitin et al. (2018) reported Setaria barbata
(Lam.) Kunth and Kalesh
& Prakash (2015) reported A.compressus as
host plants. Our finding in this
study, however, showed for the first time that Cynodon
dactylon, a perennial grass, is also used as a
larval food plant by Y. ceylonica. Before this addition, C. dactylon was known as a host plant for only Ampittia dioscorides
Fabricius, 1793, Melanitis leda L.,
1758 (Sawant 2020), and Ypthima striata (Agavekar et al.
2020).
Egg
The colour of the egg was white/dull white and not
pale blue, but other descriptions of the egg resembled that reported by van der
Poorten & van der Poorten
(2012).
Larva
We observed only four larval instars compared to five
as noted by Green (1910) and Jayasinghe & Rajapakshe
(2020). Variation in the number of
instars in Lepidoptera is relatively normal and also species dependent (Esperk et al. 2007).
The variations in geographical location, environmental conditions and
choice of different host plants may affect development (Braby
1994). These assumptions as to Ypthima ceylonica,
however, need to be further validated by future scientific studies. Four larval instars is not unusual in satyrids. For
example, Afrotropical Ypthima impura Elwes & Edwards,
1893 (Williams 2020) and Neotropical Cissia
pompilia C. & R. Felder, 1867, and Taygetis rufomarginata
Staudinger, 1888 (K. Wolfe, unpub. data) are known to
undergo only four instars.
Our observations of the first instar closely resembled
the description by Green (1910). In the
second instar, the pink base colour was not replaced by whitish green nor were
the dorsal, sub-dorsal and sub-spiracular lines replaced with dull
green as noted by Green (1910). Instead,
our second-instar larva remained nearly
the same colour as the first instar with alternate white and pink
sub-spiracular and spiracular bands. The
transition of Green’s (1910) third instar larva resembled the description of
our second instar, with the third and fourth instars matching those stages as
described by Green (1910). Additionally,
the third instar of Ypthima ceylonica closely resembled the third and fourth
instars of Ypthima huebneri
(Saji & Das 2020). Our observations
of the fourth (final) instar were completely different from the earlier
works. The fourth instar’s base colour
was pale brown with a light brown sub-spiracular band and pale brown head. Whereas the earlier works of Green (1910) and
van der Poorten & van der Poorten
(2012) reported a green base colour with a green
subdorsal band and brownish-green head.
The final instar of Y. ceylonica
closely resembled the final instars of Ypthima
singala R. Felder, 1868 (van der Poorten & van der Poorten,
2012) and Ypthima striata
(Agavekar et al., 2020).
Chrysalis
Green (1910) and van der Poorten
& van der Poorten (2012) reported two distinct
chrysalis forms from Sri Lanka: grass-green colour and pale grayish-brown. But our chrysalis from India was dull yellow
and comparatively different from those described in the earlier studies. Moreover, we noticed that the shape and
colour of the chrysalis closely matched that of Ypthima
huebneri (Saji &
Das, 2020).
Conclusion
The description of the early immature stages of
butterflies are of great value for the identification
of juveniles in the field. It also
provides supporting data for taxonomic and phylogenetic studies. In this study, the early immature stages of Ypthima ceylonica
were described in detail for the first time from India, and a new host plant
was also reported. Our observations of
the early immature stages from India had several variations from the erstwhile
descriptions from Sri Lanka. These
variations may have occurred due to geographical isolation, subspecies or
regional variation, choice of different larval food plants or variations in
environmental factors such as temperature, rainfall, relative humidity, and
photoperiod. Future morphological and
genetic studies on the early immature stages of Y. ceylonica
from different locations in India need to be performed to better understand
the reasons for such variations.
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