Temperature and Rate of Development of the Eggs of British Anura

Temperature and Rate of Development of the Eggs of British AnuraAuthor(s): Roy DouglasSource: Journal of Animal Ecology, Vol. 17, No. 2 (Nov., 1948), pp. 189-192Published by: British Ecological SocietyStable URL: http://www.jstor.org/stable/1483 .

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[ I89 ]

TEMPERATURE AND RATE OF DEVELOPMENT OF THE EGGS OF BRITISH ANURA

BY ROY DOUGLAS

(With 3 Figures in the Text)

i. INTRODUCTION

A general account of past work on temperature in relation to amphibian morphogenesis is provided by Moore (I939), who gives also a fuller bibliography. The present paper is an attempt to apply the conclu- sions of his work, which is based on American Amphibia, especially five species of Rana, to certain British species. All individuals were obtained in the south of England: the common frog, Rana temporaria L., from the Lea Valley, the common toad, Bufo bufo (L.), from Richmond Park, and the edible frog, Rana esculenta L. forma typica, from West Kent.

The habits of the three species differ considerably; Rana temporaria is moderately aquatic, but will wander some distance from water; Bufo bufo is aquatic only in the breeding season and is seldom to be taken in water during the summer; Rana esculenta, however, is the most aquatic of all the European Ranidae, being rarely found more than a few feet from the edge of a pond.

The species are not very clearly related, Rana being firmisternous and Bufo arciferous: Rana temporaria and R. esculenta are probably the most distantly related European species of their genus. All three species are very widely distributed indeed, and are very common. R. esculenta is local in Britain, and is usually considered to have been introduced (cf. Smith, I939).

2. METHODS Eggs were obtained naturally from Bufo bufo and Rana esculenta, which usually breed in the day in nature. Those of R. temporaria, which commonly breeds by night, were procured by squeezing ova from a female into a sperm suspension derived from the testes of a male crushed in about I0-20 c.c. water.

In the case of R. esculenta, the eggs used were all from one batch; some were kept at a low temperature for a few hours before being employed for the experi- ments.

Temperature was controlled by the use of lagged boxes, with or without an electric bulb for heating, kept in rooms with regulated temperatures. Differ- ences of illumination were found, in a control experi-

ment with R. temporaria, to be of negligible im- portance.

Differences of oxygenation due to temperature differences are unlikely to have been significant. Discussing Amblystoma, Detwiler & Copenhaver (I940) state: '...eggs can develop, and at a normal rate, with exceedingly low amounts of oxygen in the water' (p. 407).

Eggs, from about 6 to 20 in number, were kept in Ioo c.c. beakers in London tap-water and examined periodically. As far as possible, they were introduced shortly before the first cleavage, but, in the other cases, they were given some hours to acclimatize before significant readings were taken. The eggs of Rana esculenta were introduced a little after the first cleavage.

The stages given are those of Pollister & Moore (I937) for R. sylvatica. In all cases where times taken to reach a given stage varied, the lowest record is given. Stages 4-6 inclusive, which cannot ade- quately be plotted on a graph, and stages 8 and 9, which are not easy to define, have been omitted from all tables. Stage 7 of R. esculenta was not studied.

As in Moore's work, the number of females used is indicated in the tables, and the data for one temperature are plotted as a straight line by varying the inter- vals on the abscissa (Figs. I-3).

3. ECOLOGY AND DISTRIBUTION

R. temporaria is the most northerly of all European Anura-if not of all the Amphibia-reaching 700 N. (Boulenger, I898), and also being recorded from io,ooo ft. The southern limit is 430 N.; and in the meridional parts of its habitat it is a mountain species replaced in the plains by R. agilis and its close allies.

Near London, the common frog spawns usually in March, though occasionally in February or April. Even in ponds within a few miles of each other, however, the period of maximum spawning may vary by 2 or 3 weeks in most years (Mitcham Common, Richmond Park). Eggs of this species will develop at very low temperatures-taking more than a fortnight at 3-3 ? 0.20 C. to reach stage io. (This is a longer period than that recorded by Hertwig, I898.) They can tolerate at least I 2 hr. at o0 C.



I90 Development of eggs of British Anura

20

19

=0,~~~~~~~~~~~~~~~~~~0 17/

2 0 608o 0 2 4 6

~18 E a- 0

-17- 0

~13-

12 - Rana temporaria

11 10

20 40 60 80 100 120 140 160 Hours from first cleavage

Fig. i.

20 E 20 -

19

12 ,A / / Bufo7bufo 19 f o o

~18* 'E1 -. E E- 18 G

L i. I. I I. I I I I.II' I I I I I 204 08 0 2 4 6 8 0 2 4 6 04 0 80 100 2 4 8 0 2 4

v 17 ; 1

o16- 8'17- 15 * ~~~~~~~~~~~~~~~~~,~' 16-

13- V1

Bufo bufo 14 *Rana esculenta 12- * 13

12 10 *11

20 40 60 80 100 120 140 160.180 200 220 240 260 20 40 60 80 100 120 140 160 180 200 220 240 Hours from first cleavage Hours from first cleavage

Fig. 2. Fig. 3.

Bufo bufo is another boreal species, but less so than Rana temporaria. The northern and southern limits are respectively 650 N. and 340 N. The maximum elevation is 7000 ft. (Boulenger, I 898). Near London, spawning usually takes place about the first week in April.

The eggs are smaller than those of R. temporaria and are deposited in strings instead of batches. The

embryos leave the mucilage about stage IS or i6, instead of late in stage 20, as with Rana.

Some difficulty was experienced in identifying stages I4-I 7, because of the differences in shape from those existing in R. sylvatica. Stage i8 is character- ized by the beginning of muscular movement.

Rana esculenta. This species extends from 590 N. (Sweden) to 280 N. (Sahara), and from Japan to



RoY DOUGLAS I9I

Britain. Five subspecies are recognized. Both northern and southern limits are more southerly than those of R. temporaria or Bufo bufo.

Near London, the species normally breeds rather early in May-commonly in the first spell of hot weather-but has been known to reproduce towards the end of April.

This species is more tolerant of heat but less of cold than the others, in its early stages; spawn will develop at 28 5 ? o090 C., while it is difficult or impossible to get eggs of Rana temporaria or Bufo bufo to survive for more than a few hours above about 24-25'. On the other hand, eggs kept at a little above freezing-point for 2 days gastrulated abnormally, the blastopore lips being unable to grow round the whole yolk plug, while those kept a little longer died before the appearance of the dorsal lip. Hertwig (I898) reports 32-33' C. as the upper limiting temperature of the embryo.

4. DISCUSSION

While the three species here studied are not closely related, the verywide distribution they all possess, and their great abundance, ensures that the data given should be strictly comparable. All extend from Western Europe to Japan, and their Asiatic limits of distribution, although different from, are in the same order as, their European ones.

We have here a close correlation between development rates and various distribution factors. As Table 4 shows, the species developing most rapidly at

a temperature easily tolerated by all, also extends farthest north, is most restricted in the south, extends to the highest altitude, and, at a common latitude, breeds first. The species developing least rapidly is the opposite in all these respects, and the species intermediate in development rate is also intermediate in the other particulars.

The character of the eggs seems also to show some correlation with the other factors. Alone of European Anura, the spawn of Rana temporaria floats in water. This is presumably connected with the need to ex- ploit to the utmost the early spring sunshine in order to hasten development. Furthermore, spawn is not deposited among weeds, as is the case with the other two species; this again is probably connected with the need for solar heat and the prevention of shading by water-plants.

Bufo bufo, while differing from Rana temporaria in these respects, yet resembles it in pigmentation. In both species, the animal (i.e. the upper) half of the egg is very dark brown in colour. (IrnBufo bufo, and some- times in Rana temporaria, the vegetable pole is also deeply pigmented, but, since that is not exposed to the sun's rays, this would not seem relevant.) This pigmented surface functions as a heat-absorber, while the very pale brown animal pole of R. esculenta would serve rather to reflect heat. Since the shallow water at the edge of ponds, in which esculenta spawns, often becomes quite warm in May or June, the problem faced by this species is rather that of pre- venting the eggs from getting too hot than of ex- ploiting to the full the warmth available.

Table i. Time in hours taken for eggs of Rana temporaria to reach various stages, from time of first cleavage

No of WV used ... 3 3 3 Temperature ... 24.00?0 C. I74?? I I4? C. I3*90 +0.90 C.

Stage 7 4 5 6 I0 2Ij 25 II - 24 28 I2 27i 34i 13 29- 50

I4 54 I5 52

I 6 38j 5 5 I7 42- 72 i8 47j 68j 96 I9 6i - II7 20 651 97 I4I



I92 Development of eggs of British Anura

Table 2. Time in hours taken for eggs of Bufo bufo to reach various stages, from time of first cleavage

No. of YY used ... 4 4 3

Temperature ... 24.00?10 C. 17.60+ 1.60 C. 13.90+0-90 C.

Stage 7 5

10 - i8 40

II 21 -

12 25 - 66 13 o9

'4 44-

I5 - 58 114

i6 45 ii8 17 49 82 143 I8 55 86 I63 I9 70 III 2I6

20 74 139 257

Table 3. Time in hours taken for eggs of Rana esculenta forma typica Blgr. to reach various stages, from time of first cleavage

No. of ?? used ... I* I* I* I

Temperature ... 28'5??o09? C. 24.20? I-4? C. 20-1 00.50 C. I6-40?0?-8 C.

Stage i0o 6 I8

II -I- 21

12 10 30

I3 I9 4I 70

I4 20 - 44 75 I5 22 55 9I

i6 3I 63 I7 3I 33 67 II9

i8 46 93 I45 I9 45 55 II5 I70 20 55 69 I47 235

Compare text.

Table 4. Comparison of certain data for three Anura

Species ... ... Rana temporaria Bufo bufo Rana esculenta

Normal breeding month near March April May London

Most northerly record 700 N. 650 N. 590 N. Most southerly record 430 N. 340 N. 280 N. Maximum elevation 10,000 ft. 7000 ft. 3500 ft. Interval between stages 3 and 20 97 hr. I39 hr. 170 hr.*

at 17.60 + I -6 C. * By interpolation.

REFERENCES

Boulenger, G. A. (1897-8). 'Tailless Batrachians of

Europe.' 2 vols. Proc. Ray Soc.

Detwiler, S. R. & Copenhaver W. M. (1940). 'The

developmental behaviour of Amblystoma eggs sub-

jected to atmospheres of low oxygen and high CO2.' Amer. J. Anat. 66: 393-4I0.

Hertwig, 0. (1898). 'Ueber den Einfluss der Tem-

peratur auf die Entwicklung von Rana fusca und Rana

esculenta.' Arch. Mikr. Anat. 51: 3I9-8I.

Moore, J. A. (1939). 'Temperature tolerance and rates

of development in the eggs of Amphibia.' Ecology, 20: 459-78.

Pollister, A. W. & Moore J. A. (I937). 'Tables for the normal development of Rana sylvatica.' Anat. Rec. 68: 489-96.

Pugh, R. (I934). 'Induced ovulation and artificial fertilization in the frog.' Biol. Bull. Woods Hole, 66: 22-9.

Smith, E. P. (I939). 'On the introduction and distribution of Rana esculenta in East Kent.' J. Anim. Ecol. 8: I 68-70.



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Temperature and Rate of Development of the Eggs of British Anura