Pallas’s or Great Black-headed gull’s (Larus ichthyaetus) feeding preference for toxic Lunartail puffer (Lagocephalus lunaris)

Full text

SCIENTIFIC CORRESPONDENCE
CURRENT SCIEN CE, VOL. 111, NO. 3, 10 AUGUST 2016 4 67
might be responsible for weakening of the
monsoon over Rajasthan, causing massive
changes in the biota9,18,25.
1. Wing, S. L. and Currano, E. D., Am. J.
Bot., 2013, 100, 12 34–1254.
2. Kennett, J. P. and Stott, L. D., Na ture ,
1991 , 353 , 225–229 .
3. Thomas, E. and Shackleton, N. J., In
Corr elation of the Ea rly Paleogene in
Northwes t Europe (eds Knox, R. W. O.
B., Corfield, R. and Du nay, R. E.), Geo-
logica l Society Specia l Publication 101,
Washington DC, 1996, pp. 401–441.
4. Thomas, D. J., Zachos, J. C., Bralower,
T. J., Thomas, E. and Boha ty, S., Geo-
logy , 2002, 30 , 106 7–1070.
5. Tr ipati, A. a nd Elderfield, H ., S cien ce,
2005 , 308 , 1894–1898.
6. Zachos, J., Pagani, M., Sloan, L., Tho-
mas, E. and Billups, K., Science, 2001,
292, 686–693.
7. Zachos, J. C. et al., Science, 2003 , 302,
1551– 1554.
8. Slu ijs, A. et al., Na ture, 20 06, 441, 610–
613.
9. Shu kla, A., Mehrotra, R. C., Spi cer, R.
A., Spicer, T. E. V. and Kumar, M.,
Palaeogeogr., Palaeo clim atol ., Pa-
laeoecol., 2014, 41 2, 187–198.
10. Molnar, P. and Stock, J. M., Tectonics ,
2009 , 28 , TC3001.
11. Herendeen, P. S. and D ilcher, D. L., Ad-
vances i n Leg ume Systematics. Part 4.
The Foss il Record, T he Royal Botanic
Gardens, Ke w, 1 992.
12. Lewis, G., Schrire, B., MacKinder, B.
and Lock, M., Le gume s o f the World,
Royal Botanica l Gardens, Kew, 2005.
13. Angiosperm Phylogeny Group III, Bot.
J. Linn. Soc., 2009 , 161, 105 –121 .
14. Soltis, D. E. et al., Bot. J. Linn. Soc.,
2000 , 133 , 381–461 .
15. Wikström, N ., Savol ainen, V. and Chase,
M. W., Proc. R. Soc . London , Ser. B ,
2001 , 268 , 2211–2220.
16. Srivastava, G. and Mehr otra, R. C., J.
Geol . Soc . India, 2010, 75, 8 20–828.
17. Khan, M. A. and Bera, S., J. Geol. Soc .
India , 2014, 83, 165–174.
18. Shukla, A. a nd Mehrotra, R. C., Hist.
Biol., 2014, 26, 693 –698.
19. Polhill, R. M. and R aven, P. H. , Ad-
vances i n Leg ume Systematics, Par t 2,
Royal Botanic Gardens, Kew, 1 981.
20. Gunn, C. R., U.S.D.A. Te ch. Bull., 1984,
1681 , 1–194.
21. Goeppert, H. R., Die Ter tiarä flora
von Schossnitz in Schlesien , Gor litz,
1855 .
22. Lakhanpal, R. N. and Da yal, R., C urr.
Sci., 1966, 35 , 209–221 .
23. Lau, K. M. and Yang, S., Adv. Atmos .
Sci., 1997, 14 , 141–162 .
24. Zhang, S. P. a nd W ang, B., Int. J. Clima-
tol., 2008, 28 , 156 3–1578.
25. Prasad, V., Farooqui, A., Tripathi, S. K.
M., Garg, R. and Thakur, B., J. Biosci.,
2009 , 34 , 771–797.
26. Kutzbach, J. E., Guetter, P. J., Ru ddi-
manm, W. F. and Prellm, W. L., J. Geo-
phys. Res., 1989, 94, 18393–18407 .
27. Molnar, P., Engl and, P. and Ma rtinrod,
J., Rev. Geoph ys., 1993, 31, 357–396.
28. An, Z. S., Kut zbach, J. E., Prell, W. L.
and Porter, S. C ., Nature, 2001 , 4 11, 62–
66.
29. Spicer, R. A. et al., Nature, 2003, 421,
622–6 24.
ACKNOWLEDGEMENTS. We are gra teful
to t he a uthorities of the Venugopal Saturama n
Lignite Mi ne (VSLP), Gu rha for permitting
them to collect the fossil materi al. They also
thank the Directors of the Forest Research In-
stitu te, Dehradun and the Centr al National
Herba rium, H owrah for their p ermis sion to
consu lt the herbariu m. Tha nks are a lso due to
the Director, B irba l Sahni I nstitute of Palaeo-
sciences, Luck now for providing infrastruc-
ture facilities and permissio n to publ ish this
paper.
Receiv ed 3 Se ptember 2015; accepted 3 June
2016
ANUME HA SHUKLA
R. C. ME HROTRA*
Birbal Sahni Institute of Palaeosciences,
53 University Road,
Lucknow 226 007, India
*For correspondence.
e-mail: rcmehrotra@yahoo.com
Pallas’s or Great Black-headed gull’s (Larus ichthyaetus) feeding
preference for toxic Lunartail puffer (Lagocephalus lunaris)
More than any other group of seabirds,
gulls exploit a wide variety of food types
and have evolved highly diversified for-
aging methods and habitats1. This has
been demonstrated among gulls, both in
the family as a whole and within each
species, and at all times of the year. As a
long-distance migrant, gulls, esp ecially
in the non-breeding season, spend more
time on large water bodies along the
coasts or in the open ocean; as a result
they flourish on fish and marine inverte-
brates as their diet. Gulls in general are
thus opportunistic and omnivorous.
Pallas’s gull Larus ichthyaetus Pallas,
1773, chiefly feeds on fish and particu-
larly on dead fish1. Other feeds include
crustaceans, insects and small mammals,
less often birds and their eggs, reptiles
and seeds2. The Pallas’s gull has an ex-
tremely large distributional range. Breed-
ing range of this species extends from
the Danube Delta in Romania eastwards
across large areas of Central Asia to
western China, where the lakes of the
Qinghai–Tibet plateau hold most of the
Chinese breeding population3. The mi-
gratory route of this gull is from Central
Asia to coastal Bengal, encompassing
diverse bi ome extending from the inland
freshwater ponds, lakes to marine saline
water4. The Bay of Bengal, with exten-
sive areas of coastal mudflats, is an
important wintering site for Pallas’s gull
and other species of gulls, from early
November to mid-March5. A Pallas’s
gull captured and marked in China has
been recovered in Assam, India, i ndicat-
ing that it may possibly be using many
places in India as stopover sites4– 6. Gulls
feeding on a toxic fish species have not
been documented, but there are reports
on how the predators learn to avoid such
toxic prey7– 11. Nevertheless, a n emerging
alternati ve view is that predators should
not entirely neglect toxic prey as long as
this could increase their opportunity to
gain energy12– 15. A novel toxin-based op-
timal diet model was developed on the
basis of data on prey abundance, diet
choice, l ocal survival and number of red
knots1 6. Here we report instances of
Pallas’s gull feeding on toxic Lunartail
puffer, Lagocephalus lunaris.
Pallas’s gulls were observed from
December 2013 (post-monsoon) to May
2014 (pre-monsoon) around the coastal

SCIENTIFIC CORRESPONDENCE
CURRENT SCIEN CE, VOL. 111, NO. 3, 10 AUGUST 2016 468
areas of Purba Midnapur, West Bengal
to Talsari, Odisha located between
213322N and 872521E to
213715N and 873011E. The gull
colony primarily gathered at the southern
part of the study area, where new land
masses formed at the mouth of the River
Subarnarekha (Figure 1 a). Pallas’s gull
life phases and L. lunaris were identified
after Grimmett et al.17 and Veeruraj et
al.18 respectively. Both non-breeding
gulls (Figure 1 b) and third summer
individuals were obser ved during post-
monsoon (December–February) and
pre-monsoon (March–May) season res-
pectively. During April 2014, we noticed
one group of third summer gulls predat-
ing on Lunartail puffer (Figure 1 c and
d), even though a large number of edible
mullet fishes (Mugilidae) were also
available in the vicinity as local fisher-
men caught them using fishing nets.
After capturing the live lunartails, gulls
engulfed them wholly either in flight or
after settling down on the gr ound at a
distant place, approximately 1 km away
from the actual fishing site. Seven obser-
vations were made on the gulls feeding
on both the fresh as well as dead, decay-
ing lunartail puffers along with edible
fishes available at the site (Table 1).
Gulls had chosen fresh l unartails over
mullets on all occasions. At the same
time the gulls were also seen avoiding
dead, decaying puffers and preferred
roughly 33% of fresh mullets in their
diet.
Evidence of puffer fish intoxication
has been reported in different parts of the
world19–21. L. lunaris contains a potent
neurotoxin known as tetrodotoxin (TTX),
which has the ability to sele ctively block
the ion transport of the sodium channel22.
TTX is a colourless crystalline com-
pound (C12H17N3O10), which is slightly
soluble in water and acidic solution.
Toxicological profiles of L. lunaris were
observed along with three other puffer
fishes available from a previous study23.
The toxicity of L. lunaris was measured
to be high in the liver and ovary with
respect to the tissues, especially in the
monsoon and post-monsoon seasons dur-
ing the reproductive cycle. L. lunaris was
also recorded as the third most toxic
puffer after Chelonodon patoca and
Takifugu oblongus in the study area.
Sel ection of abundant versus rare spe-
cies can greatly alter the magnitude of a
predator’s impact on t he ecological com-
munity24. Here, the feeding behaviour of
Pallas’s gull involving fresh toxic diet
over local edible fishes, and selection of
edible fishes over decaying puffers raises
questions on the availability of food
essential for later physical development,
as well as, typical pattern of feeding
choices. Nevertheless, the possible die-
tary choices of gulls in terms of func-
tional response to the prey (prey value to
predator) remain unexplained. Though
we recorded incidences of gulls feeding
on toxic fish species only recently, how
long the Pallas’ s gulls feasted on them
and what could have been the effect re-
main unclear. Studies on Pallas’s gull s
migrating t o the east coast of India from
neighbouring China have reported that
many of them died en-route to their
breeding sites in Xinjiang, China, includ-
ing a few t hat wintered in Assam in
March 1984. Our observations of
Pallas’s gulls feeding on the toxic Lunar-
tail puffers during April 2014 and the
death of a few gull s en-route to their
breeding grounds5 around the same pe-
riod support, to some extent, the possible
link between the effect of toxic diet to
sustain long-distance migration and mor-
tality of the gulls. Though Guo-Gang et
al.5 could not establish any factors r e-
sponsible for the decline in breeding
numbers of these gulls other than degra-
dation of wetlands in their stopover sites,
our finding of gulls feeding on toxic
puffer fishes may prove to some extent
the possible adverse effect of toxic diet
in their metabolism during return migra-
tion. However, more studies are needed
to firmly establish this assumption, espe-
cially with the migrating Pallas’s gulls
from their breeding sites in China.
Furthermore, an outbreak of highly
Figure 1. a, Study area . Arrows indi cate resting pla ce o f Palla s’s gulls. (Inset) Loca
tion of the
study area on the map o f India. b, Pa llas’s gull, non-breeding. c, Palla s’s gull preda ting on lu nar-
tail puffer
, Legocep halus luna ris. d, L. lunaris cau ght by loca l fisherma n.
Table 1. Feeding prefer ence of Palla s’s gull
Observation Fresh luna r-tail pu ffer Dead, decaying lunar-tail Food preference of
no. with fr esh mullets puffer with fresh mu llets Pallas’s gull
1 + – Luna r-tail puffer
2 + – Luna r-tail puffer
3 + – Luna r-tail puffer
4 + – Luna r-tail puffer
5 – + No
6 – + Mull et
7 – + No
+, Presence; –, Absence; No, N o pre ference.

SCIENTIFIC CORRESPONDENCE
CURRENT SCIEN CE, VOL. 111, NO. 3, 10 AUGUST 2016 4 69
pathogenic avian influenza (HPAI
H5N1) in Qinghai Lake, China in 2005
resulted in the death of over 6000 water-
birds, including over 1500 gulls of two
species (Brown-headed Gull Larus brun-
nicephalus and L. ichthyaetus) in the
breeding area25. These deaths could add
to the already declining gull population,
especially in China.
1. del Hoyo, J., Elliott, A. and Sargat al, J.,
Handbook of the Bird s o f the World: Ho-
atzin to Auks, Lynx Edicions, Bercelo na,
1996 , vol. 3, p. 82 1.
2. Bir dLife International, 2014; http://
www.birdli fe.org (acce ssed on 8 Ma y
2014 ).
3. Lia o, Y. F., Wang, X., Luo, H. W. and
Liu, D. N., Chin. J. Zool., 1984, 5, 2 1–
25.
4. Muzaffar, S. et al., Forkt ail, 20 08, 24,
100–1 07.
5. Gu o-Gang, Z. et al., Fork tail , 2014, 30,
104–1 08.
6. Zang, F. Y. and Y ang, R. L., Bird Migra-
tion Research of China, Beijing Forestry
Publishing House, Chi na, 1997.
7. Gittlema n, J. L. and Harvey, P. H.,
Natu re, 1980, 286, 149–150.
8. Alatalo, R. V. and Mapp es, J., Nat ure,
1996 , 382 , 708–710 .
9. Spee d, M. P., Anim . Be hav., 2000 , 60 ,
269–2 78.
10. Greenlee s, M. J., Phillips, B. L. and
Shine, R., Behav. Ecol., 2010, 21, 966–
971.
11. Halpin, C. G. and Rowe, C., Bio l. Lett.,
2010 , 6, 617–619 .
12. Sherrat t, T . N., Speed, M. P. and Ruxton,
G. D., J. Theo r. Biol. , 2004, 228 , 217–
226.
13. Barnett, C. A., Bateson, M. and Rowe,
C., Behav . Eco l., 2007, 18, 6 45–651.
14. Skelhorn, J. and Rowe, C., Curr. Biol.,
2007 , 17 , 1479–1483 .
15. Barnett, C. A., Skelhorn, J., Bateson, M.
and R owe, C., Be hav. Eco l., 2012, 23,
418–4 24.
16. van Gils, J. A. et al., Proc. R. Soc., Lon-
don Ser. B, 2013, 2 80, 1–10.
17. Grimmett, R., Inskipp, C. a nd Inskipp,
T., Pock et Guide to the Bird s of the In-
dian Sub cont inenet, Oxford University
Press, New York , 2009, p. 384.
18. Veeruraj, A., Aru mugam, M., Aji thku -
mar, T. and Bala subra manian, T., Zoo-
taxa , 2011, 30 15, 1 –12.
19. Lange, W. R., Am. Fam. Phy sician,
1990 , 42 , 1029–1033 .
20. Ghosh, S., Hazr a, A. K., Mitra , S. K. and
Mukherjee, B., In Nutrients and Bioac-
tive Sub stan ces in Aquatic Organisms
(eds D evadasan, K. et a l.), Paico Pri nting
Press, Cochin, 1 993 , pp. 44–58.
21. Nunez-Vanzqu ez, E. J., Y otsu -
Yama shita , M. , Sierra-Beltr an, A. P.,
Yasu moto, T. and Ocha, J. L., Toxicon ,
2000 , 38 , 729–734.
22. Baselt, R., Di sposition of Toxic Drugs
and Ch emica ls in Man, Biomedical Pub-
lications, Foster City, CA, 2008, 8th edn.
23. Ghosh, S., H azra , A. K., Banerjee, S. and
Mukherjee, B., Indian J. Mar. Sci ., 2004,
33(3), 276–280 .
24. Ellis, J. C., Allen, K. E., Rom, M. S. and
Shulman, J., J . Exp. Mar. Biol . Ecol.,
2012 , 416–417 , 84–91.
25. Chen, H. et al., J. Virol., 2006, 8 0, 597 6–
5983 .
ACKNOWLEDGEMENTS. We thank the
Director, Zoological Su rvey of India for his
generous su pport . Ou r special t hanks to Mr
Ranjit Bera for his continuou s help dur ing this
study. We also thank the fishermen o f Tal sari
and the surroundings for their hel p dur ing the
study.
Receiv ed 11 February 2015; accepted 3 June
2016
TRIDI P KUMAR DATTA1
SURAJI T BHADRA ROY2
SHRUTI SENGUPTA3
ANIL MOHAPATR A1,*
G. MAHESWARAN4
1Marine Aquarium and Regional Centre,
Zoological Survey of India,
Digha 721 428, India
2Kanthalia F.P. School,
Bongaon, 24 Parganas (North),
Kanthalia 743 251, India
3Vidyasagar College,
Sankar Ghosh Lane,
Kolkata 700 006, India
4Zoological Survey of India,
New Alipore,
Kolkata 700 053, I ndia
*For correspondence.
e-mail: anil2k7@gmail.com