ISSN 1067-4136, Russian Journal of Ecology, 2016, Vol. 47, No. 6, pp. 552–556. © Pleiades Publishing, Ltd., 2016.
Plasticity in Metamorphic Traits of Rana kukunoris Tadpoles:
The Interactive Effects of Food Level and Rearing Temperature
Tong Lei Yu*, Yan Ting Han, and Shuai Peng Zhang
Department of Biology, College of Life Science, Xinyang Normal University, SD 464000 China
Received August 19, 2015
Abstract—Larval amphibians are particularly likely to encounter variation in rearing temperature and
resource availability due to variation in aquatic breeding habitats. In this study, plasticity in growth rates, lar-
val mass, larval period, and size at metamorphosis were examined in Rana kukunoris Nikolskii, 1918 under
different combinations of temperature and food level. Larval period and larval body mass was sensitive to food
level, and varied with temperature. Tadpoles metamorphosed at an older age at low temperature than those
reared at warm temperature. Food level was a significant affect on larval period at low temperature, but not
at warm temperature. Mass was heavier for tadpoles reared at low temperatures than those reared at warm
temperatures. The effect of food level depended on temperature, because larvae reared at low temperature
that were offered a high food level achieved a larger size than larvae offered a low food level, but this did not
occur at warm temperature. Therefore, we suggest that high food availability at low temperature prolonged
developmental periods, thus larvae are larger as metamorphs than those reared at warm temperatures.
Keywords: size at metamorphosis, Rana kukunoris, larval period, phenotypic plasticity, food level, rearing
In animals with complex life cycles, such as
amphibians, metamorphic size and timing are import-
ant fitness components. The quantity of food accessi-
ble during the larval stage has important effects on the
size and timing of metamorphosis (Leips and Travis,
1994). For instance, a steady food supply generally
elicits metamorphosis at a younger age and larger size,
which is generally believed to confer greater opportunity
to escape predation before and after their transition to a
terrestrial life stage. This also correlates with a younger
age and larger size at first reproduction, and thus a
potentially higher fecundity (Harris, 1999; Werner,
1986; Semlitsch et al., 1988). Moreover, large meta-
morphs may have a greater ability to withstand starva-
tion (Tracy et al., 1993; Semlitsch et al., 1999).
Larval amphibians are particularly likely to encounter
variation in rearing temperature and resource availability
due to variation in aquatic breeding habitats. Therefore,
besides energy uptake, rearing temperature can be consid-
ered the most important proximal cause of variation in size
and age at metamorphosis. Low temperatures retard dif-
ferentiation more than growth, thereby increasing stage-
specific size (Smith-Gill and Berven, 1979). As a result,
larval anurans reared at cold temperatures have prolonged
developmental periods, but they are also larger as meta-
morphs than conspecifics reared at warmer temperatures.
This phenomenon constitutes one of the most general
rules regarding ectotherms (Atkinson, 1994, 1996).
Although temperature and food level exert a strong
influence on larval growth, little is known about the
interacting effects of these factors on age and size at
metamorphosis. We examine the effects of food level and
temperature on size and age at metamorphosis of Rana
kukunoris, Nikolskii, 1918. This animal is endemic to the
eastern Tibetan plateau (29°–41° N, 93°–104° E) and is
distributed at high elevations (Zhang, 1999; Xie et al.,
2000). R. kukunoris is an explosive breeder (Wells,
1977) with a short breeding period (Yu et al., 2013). In
this study, we tested experimentally how sensitivity to
temperature and its interaction with food level has
influenced variation both in the length of larval period
and in the body size of R. kukunoris at metamorphosis.
Additionally, we discuss the potential adaptive value of
developmental plasticity in this species.
MATERIALS AND METHODS
Study Species and Rearing Condition
Egg masses of R. kukunoris were collected from one
population in Huangyuan County (36°40′ N, 101°20′ E,
altitude 2546 m), Qinghai, China, in April 2012.
The article is published in the original.