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Singers With Hot Bodies:
African Cicadas Reveal New Tricks
by Martin H. Villet, Al F. Sanborn and Polly K. Phillips
Throughout Africa, the annual arrival of summer is heralded by the singing of
the cicadas, yet few people have ever seen one of these raucous insects. A
recent collaboration between Rhodes University in Grahamstown, South Africa, and
Barry University in Florida, USA, has revealed some of the tricks that allow
these strident bugs to make such a racket without being seen, even if one
searches for them. Some of these tricks seem to be unique to African species.
Greek and Roman poets wrote of carefree cicadas singing away the summer, but
this calling activity is actually an earnest business. The cicadas are trying to
reproduce, and the songs (produced only by the male) are the means by which
males and females meet. The males' songs need to be as attractive to the females
as possible or the male may not attract a mate. We have determined that a major
group of African cicadas employs a costly method of regulating their body heat
in an effort to minimize any effect that weather could have on their song's
characteristics. This large cost is a good indication of the importance of
singing to cicadas.
To understand why they do this, one needs to remember that animal cells are
basically tiny chemical reactors and all of their chemical reactions are
temperature-dependent. The enzymes that catalyze the chemical reactions that
keep the cells alive function most efficiently over a limited range of body
temperatures. As a result, animals need to regulate their body heat to keep
their enzymes working at their optimum. Two main strategies for thermoregulation
have evolved in animals: ectothermy and endothermy.
Ectothermy is used by many diurnal animals, including many cicadas from all over
the world. Ectothermic animals use the heat of the sun to regulate their body
temperature to a range where their enzymes function efficiently. Ectotherms have
been called cold-blooded in the past, but this is inaccurate. Ectotherms can be
quite warm-bodied because they will bask in the sun to gain heat. They also seek
shade when they have are getting too hot. The animal decreases its solar heat
gain in the shade, and can therefore cool. By shuttling between sun and shade,
ectotherms can maintain their body temperature within their optimal range.
Ectothermy is an inexpensive way to regulate body temperature because the sun
provides the energy necessary. The drawback is that the sun or some other heat
source must be present for the system to work. This problem led to the evolution
of the second strategy of thermoregulation, which uses an internal heat source.
Endothermy permits activity independent of environmental temperatures, and we
have found that it occurs in a surprising number of African and New World
cicadas. They use cellular energy to generate heat, not just as a byproduct of
activity, but also specifically for thermoregulation.
As might be expected from their small body size, many African cicadas use
ectothermy, the general pattern of thermoregulation for insects. However, to our
surprise, we discovered that several African members of the cicada tribe
Platypleurini (the New World cicadas belong to other tribes) are endothermic.
Measurements of body temperature in active animals in the wild showed that Pycna
semiclara, Platypleura cf. brunnea, Pl. capensis, Pl. divisa, Pl. hirtipennis,
Pl. plumosa, and Pl. wahlbergi regulate their body temperatures to the same
range, about 36-40°C. They are not just warm-blooded, they are hot-blooded!
These species reach these temperatures even when there is no access to solar
energy, such as when there are heavy clouds, or in the evening.
Using minaturized electronic thermomenters, we have measured the body
temperatures of individuals of Pycna semiclara, Pl. capensis, Pl. hirtipennis,
and Pl. plumosa that are more than 20oC warmer than ambient temperature during
their evening choruses. Statistical analysis of the relationship between body
temperature and ambient temperature confirmed that the cicadas are
thermoregulating endothermically. By measuring its metabolic activity in the
laboratory, we have just identified Azanicada zuluensis as another endothermic
species from the same tribe. It seems that endothermy is a major
thermoregulatory strategy in the platypleurine cicadas.
Endothermic cicadas' heat is generated by their thoracic muscles. Muscle is a
good heat-generating tissue because it is highly aerobic, it makes up a
significant fraction of body mass, and it is only about 20% efficient so most of
the energy that is burned by muscle is released as heat. Even though the heat is
generated by the flight musculature, the platypleurine cicadas are able to
elevate body temperature without flight.
The first unusual feature of the African endothermic cicadas is that there are
no obvious "shivering" movements of their wings during endogenous
warm-up (as is seen in South American endothermic cicadas and in many moths).
Instead, we observed that in all of the endothermic platypleurines the abdomen
alternately extends and contracts in a telescoping fashion while the animals
warm. The rate of this abdominal pumping was temperature-dependent in
Platypleura capensis. The pumping movements probably increase respiratory
ventilation to provide the oxygen necessary for heat generation. Amongst
cicadas, this behaviour is unique to the platypleurines.
A second unique feature of the African endothermic cicadas is that, unlike
endothermic New World cicadas, many African species do not make use of solar
energy, even when it is available. This is impressive because, although
endothermy liberates animals from environmental conditions, it comes at a
significant energetic cost, particularly for
cicadas, because small animals lose heat much more rapidly than larger animals.
For this reason, small animals like cicadas must generate more heat per unit of
body mass than large animals if they are to offset their greater rate of heat
loss. For example, the endothermic African cicadas range in size from 0.376 g (Platypleura
wahlbergi) to 1.32 g (Pycna semiclara) but maintain a body temperature about the same as humans
(37°C), even when ambient temperatures are about 18°C. Simple calculations show
that this metabolic achievement is the equivalent of an unclothed human
maintaining normal body temperature in environmental conditions of -10°C.
There is an additional consideration when cicadas employ endothermy: all cicadas
feed on xylem fluid, which does not contain large amounts of energy. The use of
endothermy by cicadas will cause their energy reserves to be depleted more
rapidly. For this reason, cicadas use endothermy only when they need to be
active, and cool down to ambient temperatures at other times. This is termed
facultative endothermy.
 Of the platypleurine species we have studied, only the Eastern Cape species
Albanycada albigera is ectothermic. It is possible that A. albigera has
abandoned endothermy as it adapted to living in its Valley Bushveld habitat,
where it can obtain easy access to the sun and thermoregulate using behavioural
mechanisms. This strategy would save individuals of A. albigera significant
metabolic energy compared to an endotherm, potentially increasing their adult
life span. In contrast, many of the other platypleurine species call from under
the canopy of their host plants, often in shady forest habitats.
Many African platypleurines benefit from endothermy in several ways by calling
from the trunk and primary branches of forest trees. First, most cicadas have
clear, glassy wings, but platypleurines are unusual in having a mottled
colouration pattern on their bodies and beautifully pigmented wings that allow
them to hide among the mosses and lichens on the bark, making it difficult for
predators to locate the cicada. The cicadas are able to make better use of these
highly camouflaged colour patterns by calling from the shaded understory of
their host plants, where visibility is poorer. Unlike New World endothermic
cicadas, African endothermic platypleurines tend to avoid patches of sunlight
that could provide radiant energy to facilitate thermoregulation.
This
behaviour supports the contention that platypleurines try to avoid detection on
the trunks and primary branches, and explains why they can be so hard to see,
even if you are searching for them. In addition, calling from the more open
trunk and branches may decrease competition for calling sites with ectothermic
species because ectotherms require access to sunlight and are therefore
restricted to the canopy where they
can maintain body temperature. Finally, calling from the open spaces in the
understory may also make it easier for the female to locate the male.
Another benefit of endothermy in cicadas is that it provides them with
independence from environmental conditions. Dawn and dusk chorusing, calling
when the sky is overcast, or calling when ambient temperatures are cool, are all
possible when an animal exhibits endothermic behaviour.
These cicadas are able
to continue activity regardless of environmental conditions, and can coordinate
activity to increase potential interactions between males and females. Dawn and
dusk chorusing also provides benefits to the cicadas. Sound travels a greater
distance at dawn and dusk, increasing the broadcast range of the cicadas' calls.
This will increase the potential number of mates an individual cicada can find.
In addition, the foraging success of predators like birds and mammals decreases
when light levels are low. By calling at dawn and dusk, when predator foraging
efficiency is low, cicadas can find mates and simultaneously decrease their
chances of becoming prey.
We mentioned that the males' songs need to be as attractive to the females as
possible. Each species has its own song, and females have preferences for an
ideal example of their species' song. Males may struggle to produce this ideal
song because of the effects of body temperature on the performance of their
singing muscles. Colder muscles contract more slowly, producing calls with
slower pulse rates. Such effects have been shown in the European cicada Cicada
orni, and similar effects are found in ectothermic crickets, where their rate of
chirping depends on the temperature of their surroundings. Because endothermic
cicadas are essentially independent of their thermal environment, they can
regulate the temperature of their singing muscles so that their call
characteristics are much less variable than in ectothermic species. This allows
males to compete more effectively for mates, and makes this competition more
intense. Using computer-based analysis of the call characteristics of Pycna
semiclara, we were able to confirm that they were unrelated to ambient
temperatures.
Our studies imply that endothermy could be an important thermoregulatory
strategy linked to many aspects of the biology of a major group of African
cicadas. We are now trying to determine how widespread endothermy is in the
platypleurine cicadas and what could have led to the evolution of endothermy as
a major thermoregulatory strategy. We were excited to discover endothermy in a
new tribe of cicadas, and the list of surprises has continued to grow - African
cicadas have their own way of doing things!
For more information:
Contact Professor Martin Villet, Rhodes University, South Africa at : m.villet@ru.ac.za
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