Apparent parthenogenetic reproduction in Collembola has sometimes been attributed to accidental transfer of spermatophores with the food material from one culture to another (Schaller, 1953; Mayer, 1957). Conclusive evidence of parthenogenesis has only in recent years been accumulated for a number of species of Collembola, of which some were found in field populations consisting entirely of females (Choudhuri, 1958; Huther, 1961; Marshall and Kevan, 1962; Petersen, 1965; 1971 ; Snider, 1973). In Onychiuridae, parthenogenesis is apparently quite common. Onychiurus parthenogeneticus Choudhuri and Tullbergia krausbaueri (Bomer) undoubtedly reproduce in the absence of males (Choudhuri, 1958; Hale, 1966; Petersen, 1971); so does Tullbergia granulata Mills, where individuals reared in isolation from the time of hatching invariably lay viable eggs (unpublished observations). Large females of Onychiurus procampatus Gisin 1956 breed through a form of thelytokous parthenogenesis (Hale, 1964). The size groupings found in O. procarnpatus (two sizes of females and only small males) were also observed in O. firnatus Gisin 1952 and O. quadriocellatus Gisin 1947 and may indicate the existence of both parthenogenetic and sexually reproducing forms in these species (Hale, 1964).
Recent laboratory observations on Protaphorura armatus (Tullberg) revealed that this species too reproduces parthenogenetically. The present study was undertaken to investigate the effect of temperature on the biology of the species

Snider, Renate M.

English

Valparaiso University

The Great Lakes Entomologist Volume 7 Number 1 -- Spring 1974 Number 1 -- Spring 1974 Article 3 March 1974 The Life Cycle Relative to Temperature of Protaphorura Armatus (Tullberg) (Collembola: Onychiuridae), a Parathenogenetic Species Renate M. Snider Michigan State University Follow this and additional works at: https://scholar.valpo.edu/tgle  Part of the Entomology Commons Recommended Citation Snider, Renate M. 1974. "The Life Cycle Relative to Temperature of Protaphorura Armatus (Tullberg) (Collembola: Onychiuridae), a Parathenogenetic Species," The Great Lakes Entomologist, vol 7 (1) Available at: https://scholar.valpo.edu/tgle/vol7/iss1/3 This Peer-Review Article is brought to you for free and open access by the Department of Biology at ValpoScholar. It has been accepted for inclusion in The Great Lakes Entomologist by an authorized administrator of ValpoScholar. For more information, please contact a ValpoScholar staff member at scholar@valpo.edu. 1974 THE GREAT LAKES ENTOMOLOGIST 9 THE LIFE CYCLE RELATIVE TO 'TEMPERATURE OF PROTAPHORURA ARMATUS (TULLBERG) (COLLEMBOLA: ONYCHIURIDAE), A PARTHENOGENETIC SPECIES1 Renate M. Snider Department of Entomology, Michigan State University, East Lansing, Mich. 48823 Apparent parthenogenetic reproduction in Collembola has sometimes been attributed to accidental transfer of spermatophores with the food material from one culture to another (Schaller, 1953; Mayer, 1957). Conclusive evidence of parthenogenesis has only in recent years been accumulated for a number of species of Collembola, of which some were found in field populations consisting entirely of females (Choudhuri, 1958; Huther, 1961; Marshall and Kevan, 1962; Petersen, 1965; 1971 ; Snider, 1973). In Onychiuridae, parthenogenesis is apparently quitc common. Onychiurus parthenogeneticus Choudhuri and Tlrllbergia krausbaueri (Bomer) undoubtedly reproduce in the absence of males (Choudhuri, 1958; Hale, 1966; Petersen, 1971); so does Tullbergia granulata Mills, where individuals reared in isolation from the time of hatching invariably lay viable eggs (unpublished observations). L a g e  females of Onychiurus procampatus Gisin 1956 breed through a form of thelytokous parthenogenesis (Hale, 1964). The size groupings found in 0. procarnpatus (two sizes of females and only small males) were also observed in 0. firnatus Gisin 1952 and 0. quadriocellatus Gisin 1947 and may indicate the existence of both parthenogenetic and sexually reproducing forms in these species (Hale, 1964). Recent laboratory observations on  Protaphorura armatus (Tullberg) revealed that this species too reproduces parthenogenetically. The present study was undertaken to investigate the effect of temperature on the biology of the species. MATERIALS AND METHODS Clear plastic jars (3.5 X 2.5 cm) were used as culture containers. They were filled to a depth of 1 cm with a plaster-charcoal substrate. Brewer's yeast was provided as food. Distilled water was addcd when required in order to maintain a humidity of closc to 100 percent. Whenever regular scraping of the substrate surface did not  suffice to kecp the jars free of mold, the animals were transferred to a new container. From Protaphorrrra arnlatus stock cultures, single eggs were transferred to each of a number of containers and incubated at  15"; 21"; and 26°C. Upon emergence of the juveniles, observations were made at 24 hour intervals throughout the life of the animals. Exuvia were recorded and removed from the containers. Deaths were recorded and the specimens preserved in alcohol. All eggs laid were left in the jars and allowed to hatch. At each temperature, the progeny of 15 parent individuals were reared to maturity and preserved for later sex determination. MORTALITY, LONGEVITY, INSTAR DURATION Figure 1 illustrates the survival pattern of P. arnuztus at 15', 21° and 26°C. While juvenile mortality was highest at 26'C, the over-all survival patterns at 26O and 21°C were cIosely similar. At 15"C, 50% survival was reached in 345 days. Average longevity was 320 days at  15'C, but  only 139 and 129 days at 2 1" and 26°C respectively. Table 1 summarizes the data on  duration of the stadia at  the three test temperatures. At all temperatures the first instar stadium was of shorter duration than any of the subsequent stadia. At 15°C the duration of the stadia was considerably longer than at 21°C or 26"C, while differences between the length of the stadia at 2 l0and  26°C were only slight. At all temperatures the number of days between moults gradually increased with progressing age. The mean number of instars in a life time was 23  at  15'C and 20 at  both 21" and 26°C. - ' ~ i c h i ~ a n  Agricultural Experiment Station Journal Article Number 6426. 1Snider: The Life Cycle Relative to Temperature of Protaphorura Armatus (TPublished by ValpoScholar, 197410 THE GREAT LAKES ENTOMOLOGIST Vol. 7, No. 1 I PROTAPHORURA ARMATUS TIME IN DAYS Fig. 1 .  Survival of Protaphorura urntatus (Tullberg) at three temperatures. The moulting process in juveniles and young adults was normally completed within a period of 24 hours. However, from the 10th or 12th instar on,  ecdysis often lasted from 2 to 5 days, during which the anjinals remained in one place and took no food. A drop of water placed on or beside them usually released the exuvia without injury to the animal. In sevcral very old indlv~duals ecdysis lasted from 5 to 1 0  days and sometimes resulted in death of the animal. Table 1. Average duration of selected stadia of Protaphorura armatus at three temperatures. 15°C 21°C 26" C Instar Mean Range No. repl. Mean Range No. repl. Mean Range No. repl. 2The Great Lakes Entomologist, Vol. 7, No. 1 [1974], Art. 3https://scholar.valpo.edu/tgle/vol7/iss1/31974 THE GREAT LAKES ENTOMOLOGIST 11 This extended duration of the moulting process was observed at all temperatures. At 26°C itoccurred first in a 55 day old individual (10th instar), at 21°C in a 6 3  day old animal (12th instar), and a t  15'C in a 136 day old individual (12th instar). EGG PRODUCTlON All observed individuals of P. arnmtus originated from isolated eggs and, with few exceptions, laid viable eggs at least once during their adult life. Microscopical examiflation of the specimens after death revealed that even the non-laying individuals were all females. At least in the laboratory, evidence of parthenogenesis in P. arrnatus was conclusive. Specimens collected from Michigan agricultural and forest soils have so far also been all female. However, sampling has not  been extensive; the existence of entirely female populations of P. arrnatus in the field has yet to be established. As in several other species of Collembola (Hale, 1965; Waldorf, 1971a; Snider, 1973) a close relationship between moulting and oviposition was found in P. armatus. The time interval elapsing between ecdysis and oviposition however varied with the temperature. At 26°C oviposition generally occurred within 1-2 days of ecdysis, while at 15OC the interval was commonly 2-4 days. In cases where the moulting process lasted for several days, oviposition was delayed accordingly, although a few females laid eggs while the exuvia was still attached t o  the dorsal end of the abdomen. P. arrnatus lays clumps of smooth white eggs, often in holes or against the container wall. The earliest that eggs were laid was a t  the beginning of the 5 th  instar, but initiation of egg production varied with the individual. There appeared to be no  pattern in the sequence of ovipositions. Many individuals laid eggs in each of 8 t o  12  successive instars; others produced eggs at variable intervals, with 1 to 5 and rarely more than 6 nonproductive instars intervening. The total number of ovipositions by one female ranged from 1 t o  22, with a maximum of 20 ovipositions a t  15°C and 22 at 21°C and 26°C. On the average, a female oviposited 9 times at 15°C; 9.5 times at 2I0C; and 11.5 times a t  26OC. Eggs produced during one oviposition were invariably laid in one single clump. At all temperatures the number of eggs per laying period (and clump) increased gradually up t o  the 6th ovipositlon and remained fairly constant over the next 7 or 8 ovipositions. Although the mean number of laying periods was lowest a t  15'C, the average number of eggs per oviposition per laying female was highest a t  that temperature (Fig. 2). The total number of eggs laid by one female in a life time varied from 1 t o  298. Average egg production per female as well as clump size were highest at 15'C and lowest a t  26°C (Table 2). Taking into consideration the total number of females alive at a given time, the effect of temperature on  the reproductive rate was revealed in an unexpected way. In a given instar, a smaller proportion of females was reproducing at 15' than at 21° or 26'C (Table 3). Accordingly, fecundity averages were sometimes lowcst a t  1 S°C. Cumulation of OVlPOSlTlOll  PERIODS Fig. 2.  Average egg production per oviposition and female of Protaphorura a r m a t u s  (Tullberg) at three temperatures. 3Snider: The Life Cycle Relative to Temperature of Protaphorura Armatus (TPublished by ValpoScholar, 19741 2  THE GREAT LAKES ENTOMOLOGIST Vol. 7, No. 1 Table 2. Total egg production and clump size per female of Protaphorura armatus at three temperatures. Total no. of eggs (average/female) 123.8 102.6 98.1 ' Range 7-289 1-298 13-262 Max. no. of eggs per clump 30 24 22 Average clump size 13.7 10.8 , 8.6 * fecundity means per instar demonstrates the interaction between clump size and percentage of laying females (Fig. 3). A temperature of 26"C, although inducing egg production in a high number of females, also reduces the number of eggs laid (136.4 total). At 21°C the number of eggs laid is higher, combined with a high percentage of productive females (150.7 eggs total). At lS°C the low number of egg laying females at fust reduces fecundity below the 21" level; but  the large size of the clumps finally balances average fecundity to a point where it reaches the 21" values (147.8 total). Of the original 150 individuals of P. armatus used in this study, 131 reached maturity. Over 1200 of their progeny, taken from cultures at all experimental temperatures, were reared to maturity and preserved. Microscopical examination revealed that all individuals of this second generation were again females. EGG CANNIBALISM Egg cannibalism has been observed in several species of Collembola. Green (1964) showed that in Folsomia candida (Willem) cannibalism was independent of population density. Vail (1965) observed that faulty eggs were more prone to consumption than normal eggs in cultures of Hypogastrura i?ianuhrialis Tullberg. Recently, Waldorf (1971b) demonstrated for Sinella curviseta Brook a pronounced selectivity in egg cannibalism: Table 3. Average fecundity per instar and female of Protaphorura arnzatus at three temperatures, up to the 20th instar. 15°C 21°C 26°C Ave. No. fem. 7% fem. Ave. No. fem. %fern. Ave. No. fem. %fern. lnstar eggs alive laying eggs alive laying eggs alive laying 4The Great Lakes Entomologist, Vol. 7, No. 1 [1974], Art. 3https://scholar.valpo.edu/tgle/vol7/iss1/3THE GREAT LAKES ENTOMOLOGIST Fig. 3. Cun~ulative average fecundity of Protuphoturu armatus (Tullberg) at three tern- peratures. young, smooth eggs were preferred to rough eggs in advanced stages of development. In P. armatus cannibalism occurred frequently. As in S. curviseta, only young eggs with intact chorion were ingested. Once the chorion had ruptured the eggs were no longer subject to cannibalistic attack. Owing to 24 hour intervals between observations, consumption of eggs immediately after oviposition could not  be accurately determined. Where eggs were only partially ingested, the visible remains of egg shells were included in the egg counts. Possible consumption of whole eggs or entire clumps in those first 24 hours and resulting errors in fecundity and cannibalism .data had to be disregarded. Egg cannibalism proved to be considerable at all temperatures. At 15' and 26"C, 11 percent of all observed eggs were eaten. At 21°C cannibalism was slightly less with only 7 percent of all eggs consumed. The age of the parent did not influence the rate of ingestion. Eggs were subjcct to predation at any time from the first to the last oviposition in the life of a female. In most egg clumps there were one to a few eggs that never developed, although at first they could not be distinguished from the rest of the clump. P. armatus also laid eggs that were distinctly faulty at first glance: they assumed neither the spherical shape nor the opaque white appearance of freshly laid eggs and were often deposited in amorphous masses. The females seemed unable to discriminate between such faulty eggs and healthy young eggs, since both were ingested. On the other hand, both types of eggs often remained untouched until they either hatched or deteriorated. Thus egg cannibalism affected only young eggs, but was otherwise erratic and indiscriminate. Lack of a required nutritional component in thc diet may have been the cause for both the cannibalistic behaviour and the production of faulty eggs in P. armatus. However, no food substances other than yeast were used in the investigation. EGG VIABILITY Aside from cannibalistic attack by the fcmales, eggs of P. arrmtus were also found to be susceptible to excessive fungal and bacterial contamination. Fungal growth was particulaly heavy at 26"C, in spite of constant efforts to keep the jars clean. Many egg clunlps were therefore not suited for precise counts of egg viability, including those which had been only partially ingested or were partly overgrown by fungi. At each temperature over-all data on hatching success were finally derived from egg clumps which showed no fungal infection and had not been attacked by the parent. Eggs laid at 15°C had a higher percentage of viability than those laid a t  21' and 26°C (Table 5Snider: The Life Cycle Relative to Temperature of Protaphorura Armatus (TPublished by ValpoScholar, 197414 THE GREAT LAKES ENTOMOLOGIST Vol. 7,  No. 1 Table 4. Viability of e g s  of l+otaphorura armatus at  three temperatures. No. of eggs 1216 1062 8 84 No. hatched 949 719 567 Percent 78.0 67.7 64.1 4). At least under laboratory conditions, large clump size and high egg viability may possibly compensate for the low percentage of females reproducing at lS°C. The over-all viability figures given in Table 4 are probably an overestimate, since data on faulty eggs were treated separately. At 26"C, 4.5Y of all eggs laid were faulty and clearly non-viable, as compared to 3.1% at 21°C and 3.5% at 15°C. SUMMARY Laboratory observations on  Protaphorura armatus (Tullberg) disclosed parthenogenetic reproduction in the species. Males have as yet not been found in either the stock cultures or among specimens collected from Michigan soil samples. Isolated individuals of P. armatus were reared at 15', 21' and 26°C. Longevity and survival were greatly extended at  lS°C, at which temperature the duration of the stadia was longest. Eggs were laid in clumps within a few days of ecdysis. The largest clumps were recorded at  ISo, but  at  that temperature a lower percentage of females laid eggs than at  21' or 26°C. Eggcannibalism occurred frequently and affected both healthy and faulty young eggs. ACKNOWLEDGMENTS I am indebted to Dr. Richard J. Snider for criticism and encouragement, and to Dr. James W. Butcher for providing the necessary facilities for this study, which was carried out under the Department of Entomology Soil Biology Program at  Michigan State University. LITERATURE CITED Choudhuri, D. K. 1958. On two new species of Onychiurus Gervais (Collembola: Onychiuridae) froin the British Isles. Proc. R. Entomol. Soc. London (B) 27:155-159. Green, C. D. 1964. The effect of crowding upon the fecundity of Folsonlia candida (William) var. distincta (Bagnall) (Collembola). Entomol. Exp. e t  Appl. 7:62-70. Hale, W. G. 1964. Experimental studies on  the taxonomic status of some members of the Onychiurus armatus species group. Rev. Ecol. Biol. Sol 1(3):501-510. Hale, W. G. 1965. Observations on the breeding biology of Collembola. Pedobiologia 5:146-152, 161-177. Hale, W. G. 1966. The Collembola of the Moore House National Nature Reserve, Westmoreland: a moorland habitat. Rev. Ecol. Biol. Sol 3(1):97-122. Huther, W. 1961. Oekologische Untersuchungen uber die 1:auna ppdlzischer Wein- bergsboden. Zool. Jahrb. Syst. 89:243-368. Marshall, V. G. and Kevan, D. K. McE. 1962. Preliminary observations o n  the biology of Folsomia candida Willem, 1902 (Collembola: Isotomidae). Can. Entomol. 94575-586.  Mayer, H. 1957. Zur Biologie und Ethologie einheimischcr Collembolen. Zool. Jahrb. Syst. 85:501-570. Petersen, H. 1965. The Collembola of the Hansted Reserve, Thy, North Jutland. Taxonomy, Ecology. Entomol. Medd. 30: 3 13-395. Petersen, H. 1971. Parthenogenesis in two common species of Collembola: Tullhrrgia krausbaueri (Borner) and Isotoma rzotabilis Schaffer. Rev. Ecol. Biol. Sol 8(1):133-138. Schaller, 1:. 1953. Untersuchungen zur Fortpflanzungsbiologje Arthropleoner Col- lembolen. Z. Morph. Oekol. Tiere. 41:265-277. 6The Great Lakes Entomologist, Vol. 7, No. 1 [1974], Art. 3https://scholar.valpo.edu/tgle/vol7/iss1/31974 THE GREAT LAKES ENTOMOLOGIST 15 Snider, R. M. 1973. Laboratory observatior~s on the biology of Folsornia ca~zdida (Willem) (Collembola: Isotomidae). Rev. Ecol. Biol. Sol 10(1):103-124. Vail, P. V. 1965. Colonization of Hypogastrura rnarzubrialis (Collembola: Poduridae) with notes on its biology. Ann. Entornol. Soc. Amcr. 58(4):555-561. Waldorf, E. S. 1971a. The reproductive biology of Sinella curviseta (Collembola: Entomobryidae) in laboratory culture. Rev. Ecol. Biol. Sol 8(3):451-463. Waldorf, E. S. 1971b. Selective egg cannibalism in Sinella curvlseta (Collernbola: Entomobryidae). Ecology 52(4):673-675. 7Snider: The Life Cycle Relative to Temperature of Protaphorura Armatus (TPublished by ValpoScholar, 1974

The Life Cycle Relative to Temperature of Protaphorura Armatus (Tullberg) (Collembola: Onychiuridae), a Parathenogenetic Species

ValpoScholar

The Great Lakes Entomologist 
Volume 7 
Number 1 -- Spring 1974 Number 1 -- Spring 
1974 
Article 3 
March 1974 
The Life Cycle Relative to Temperature of Protaphorura Armatus 
(Tullberg) (Collembola: Onychiuridae), a Parathenogenetic 
Species 
Renate M. Snider 
Michigan State University 
Follow this and additional works at: https://scholar.valpo.edu/tgle 
 Part of the Entomology Commons 
Recommended Citation 
Snider, Renate M. 1974. "The Life Cycle Relative to Temperature of Protaphorura Armatus (Tullberg) 
(Collembola: Onychiuridae), a Parathenogenetic Species," The Great Lakes Entomologist, vol 7 (1) 
Available at: https://scholar.valpo.edu/tgle/vol7/iss1/3 
This Peer-Review Article is brought to you for free and open access by the Department of Biology at ValpoScholar. 
It has been accepted for inclusion in The Great Lakes Entomologist by an authorized administrator of ValpoScholar. 
For more information, please contact a ValpoScholar staff member at scholar@valpo.edu. 
1974 THE GREAT LAKES ENTOMOLOGIST 9 
THE LIFE CYCLE RELATIVE TO 'TEMPERATURE OF 
PROTAPHORURA ARMATUS (TULLBERG) (COLLEMBOLA: 
ONYCHIURIDAE), A PARTHENOGENETIC SPECIES1 
Renate M. Snider 
Department of Entomology, Michigan State University, East Lansing, Mich. 48823 
Apparent parthenogenetic reproduction in Collembola has sometimes been attributed 
to accidental transfer of spermatophores with the food material from one culture to 
another (Schaller, 1953; Mayer, 1957). Conclusive evidence of parthenogenesis has only 
in recent years been accumulated for a number of species of Collembola, of which some 
were found in field populations consisting entirely of females (Choudhuri, 1958; Huther, 
1961; Marshall and Kevan, 1962; Petersen, 1965; 1971 ; Snider, 1973). In Onychiuridae, 
parthenogenesis is apparently quitc common. Onychiurus parthenogeneticus Choudhuri 
and Tlrllbergia krausbaueri (Bomer) undoubtedly reproduce in the absence of males 
(Choudhuri, 1958; Hale, 1966; Petersen, 1971); so does Tullbergia granulata Mills, where 
individuals reared in isolation from the time of hatching invariably lay viable eggs 
(unpublished observations). L a g e  females of Onychiurus procampatus Gisin 1956 breed 
through a form of thelytokous parthenogenesis (Hale, 1964). The size groupings found in 
0. procarnpatus (two sizes of females and only small males) were also observed in 0. 
firnatus Gisin 1952 and 0. quadriocellatus Gisin 1947 and may indicate the existence of 
both parthenogenetic and sexually reproducing forms in these species (Hale, 1964). 
Recent laboratory observations on  Protaphorura armatus (Tullberg) revealed that this 
species too reproduces parthenogenetically. The present study was undertaken to 
investigate the effect of temperature on the biology of the species. 
MATERIALS AND METHODS 
Clear plastic jars (3.5 X 2.5 cm) were used as culture containers. They were filled to a 
depth of 1 cm with a plaster-charcoal substrate. Brewer's yeast was provided as food. 
Distilled water was addcd when required in order to maintain a humidity of closc to 100 
percent. Whenever regular scraping of the substrate surface did not  suffice to kecp the 
jars free of mold, the animals were transferred to a new container. 
From Protaphorrrra arnlatus stock cultures, single eggs were transferred to each of a 
number of containers and incubated at  15"; 21"; and 26°C. Upon emergence of the 
juveniles, observations were made at 24 hour intervals throughout the life of the animals. 
Exuvia were recorded and removed from the containers. Deaths were recorded and the 
specimens preserved in alcohol. All eggs laid were left in the jars and allowed to hatch. 
At each temperature, the progeny of 15 parent individuals were reared to maturity and 
preserved for later sex determination. 
MORTALITY, LONGEVITY, INSTAR DURATION 
Figure 1 illustrates the survival pattern of P. arnuztus at 15', 21° and 26°C. While 
juvenile mortality was highest at 26'C, the over-all survival patterns at 26O and 21°C were 
cIosely similar. At 15"C, 50% survival was reached in 345 days. Average longevity was 
320 days at  15'C, but  only 139 and 129 days at 2 1" and 26°C respectively. 
Table 1 summarizes the data on  duration of the stadia at  the three test temperatures. 
At all temperatures the first instar stadium was of shorter duration than any of the 
subsequent stadia. At 15°C the duration of the stadia was considerably longer than at 
21°C or 26"C, while differences between the length of the stadia at 2 l0and  26°C were 
only slight. At all temperatures the number of days between moults gradually increased 
with progressing age. The mean number of instars in a life time was 23  at  15'C and 20 at  
both 21" and 26°C. 
- 
' ~ i c h i ~ a n  Agricultural Experiment Station Journal Article Number 6426. 
1
Snider: The Life Cycle Relative to Temperature of Protaphorura Armatus (T
Published by ValpoScholar, 1974
10 THE GREAT LAKES ENTOMOLOGIST Vol. 7, No. 1 
I 
PROTAPHORURA ARMATUS 
TIME IN DAYS 
Fig. 1 .  Survival of Protaphorura urntatus (Tullberg) at three temperatures. 
The moulting process in juveniles and young adults was normally completed within a 
period of 24 hours. However, from the 10th or 12th instar on,  ecdysis often lasted from 
2 to 5 days, during which the anjinals remained in one place and took no food. A drop 
of water placed on or beside them usually released the exuvia without injury to the 
animal. In sevcral very old indlv~duals ecdysis lasted from 5 to 1 0  days and sometimes 
resulted in death of the animal. 
Table 1. Average duration of selected stadia of Protaphorura armatus at three temperatures. 
15°C 21°C 26" C 
Instar Mean Range No. repl. Mean Range No. repl. Mean Range No. repl. 
2
The Great Lakes Entomologist, Vol. 7, No. 1 [1974], Art. 3
https://scholar.valpo.edu/tgle/vol7/iss1/3
1974 THE GREAT LAKES ENTOMOLOGIST 11 
This extended duration of the moulting process was observed at all temperatures. At 
26°C itoccurred first in a 55 day old individual (10th instar), at 21°C in a 6 3  day old 
animal (12th instar), and a t  15'C in a 136 day old individual (12th instar). 
EGG PRODUCTlON 
All observed individuals of P. arnmtus originated from isolated eggs and, with few 
exceptions, laid viable eggs at least once during their adult life. Microscopical examiflation 
of the specimens after death revealed that even the non-laying individuals were all 
females. At least in the laboratory, evidence of parthenogenesis in P. arrnatus was 
conclusive. Specimens collected from Michigan agricultural and forest soils have so far 
also been all female. However, sampling has not  been extensive; the existence of entirely 
female populations of P. arrnatus in the field has yet to be established. 
As in several other species of Collembola (Hale, 1965; Waldorf, 1971a; Snider, 1973) 
a close relationship between moulting and oviposition was found in P. armatus. The time 
interval elapsing between ecdysis and oviposition however varied with the temperature. At 
26°C oviposition generally occurred within 1-2 days of ecdysis, while at 15OC the interval 
was commonly 2-4 days. In cases where the moulting process lasted for several days, 
oviposition was delayed accordingly, although a few females laid eggs while the exuvia 
was still attached t o  the dorsal end of the abdomen. 
P. arrnatus lays clumps of smooth white eggs, often in holes or against the container 
wall. The earliest that eggs were laid was a t  the beginning of the 5 th  instar, but initiation 
of egg production varied with the individual. There appeared to be no  pattern in the 
sequence of ovipositions. Many individuals laid eggs in each of 8 t o  12  successive instars; 
others produced eggs at variable intervals, with 1 to 5 and rarely more than 6 
nonproductive instars intervening. 
The total number of ovipositions by one female ranged from 1 t o  22, with a 
maximum of 20 ovipositions a t  15°C and 22 at 21°C and 26°C. On the average, a female 
oviposited 9 times at 15°C; 9.5 times at 2I0C; and 11.5 times a t  26OC. 
Eggs produced during one oviposition were invariably laid in one single clump. At all 
temperatures the number of eggs per laying period (and clump) increased gradually up t o  
the 6th ovipositlon and remained fairly constant over the next 7 or 8 ovipositions. 
Although the mean number of laying periods was lowest a t  15'C, the average number 
of eggs per oviposition per laying female was highest a t  that temperature (Fig. 2). The 
total number of eggs laid by one female in a life time varied from 1 t o  298. Average egg 
production per female as well as clump size were highest at 15'C and lowest a t  26°C 
(Table 2). 
Taking into consideration the total number of females alive at a given time, the effect 
of temperature on  the reproductive rate was revealed in an unexpected way. In a given 
instar, a smaller proportion of females was reproducing at 15' than at 21° or 26'C 
(Table 3). Accordingly, fecundity averages were sometimes lowcst a t  1 S°C. Cumulation of 
OVlPOSlTlOll  PERIODS 
Fig. 2.  Average egg production per oviposition and female of Protaphorura a r m a t u s  
(Tullberg) at three temperatures. 
3
Snider: The Life Cycle Relative to Temperature of Protaphorura Armatus (T
Published by ValpoScholar, 1974
1 2  THE GREAT LAKES ENTOMOLOGIST Vol. 7, No. 1 
Table 2. Total egg production and clump size per female of Protaphorura armatus at 
three temperatures. 
Total no. of eggs 
(average/female) 123.8 102.6 98.1 
' Range 7-289 1-298 13-262 
Max. no. of eggs 
per clump 30 24 22 
Average clump size 13.7 10.8 , 8.6 
* 
fecundity means per instar demonstrates the interaction between clump size and 
percentage of laying females (Fig. 3). A temperature of 26"C, although inducing egg 
production in a high number of females, also reduces the number of eggs laid (136.4 
total). At 21°C the number of eggs laid is higher, combined with a high percentage of 
productive females (150.7 eggs total). At lS°C the low number of egg laying females at 
fust reduces fecundity below the 21" level; but  the large size of the clumps finally 
balances average fecundity to a point where it reaches the 21" values (147.8 total). 
Of the original 150 individuals of P. armatus used in this study, 131 reached maturity. 
Over 1200 of their progeny, taken from cultures at all experimental temperatures, were 
reared to maturity and preserved. Microscopical examination revealed that all individuals 
of this second generation were again females. 
EGG CANNIBALISM 
Egg cannibalism has been observed in several species of Collembola. Green (1964) 
showed that in Folsomia candida (Willem) cannibalism was independent of population 
density. Vail (1965) observed that faulty eggs were more prone to consumption than 
normal eggs in cultures of Hypogastrura i?ianuhrialis Tullberg. Recently, Waldorf (1971b) 
demonstrated for Sinella curviseta Brook a pronounced selectivity in egg cannibalism: 
Table 3. Average fecundity per instar and female of Protaphorura arnzatus at three 
temperatures, up to the 20th instar. 
15°C 21°C 26°C 
Ave. No. fem. 7% fem. Ave. No. fem. %fern. Ave. No. fem. %fern. 
lnstar eggs alive laying eggs alive laying eggs alive laying 
4
The Great Lakes Entomologist, Vol. 7, No. 1 [1974], Art. 3
https://scholar.valpo.edu/tgle/vol7/iss1/3
THE GREAT LAKES ENTOMOLOGIST 
Fig. 3. Cun~ulative average fecundity of Protuphoturu armatus (Tullberg) at three tern- 
peratures. 
young, smooth eggs were preferred to rough eggs in advanced stages of development. In 
P. armatus cannibalism occurred frequently. As in S. curviseta, only young eggs with 
intact chorion were ingested. Once the chorion had ruptured the eggs were no longer 
subject to cannibalistic attack. 
Owing to 24 hour intervals between observations, consumption of eggs immediately 
after oviposition could not  be accurately determined. Where eggs were only partially 
ingested, the visible remains of egg shells were included in the egg counts. Possible 
consumption of whole eggs or entire clumps in those first 24 hours and resulting errors in 
fecundity and cannibalism .data had to be disregarded. 
Egg cannibalism proved to be considerable at all temperatures. At 15' and 26"C, 11 
percent of all observed eggs were eaten. At 21°C cannibalism was slightly less with only 7 
percent of all eggs consumed. The age of the parent did not influence the rate of 
ingestion. Eggs were subjcct to predation at any time from the first to the last 
oviposition in the life of a female. 
In most egg clumps there were one to a few eggs that never developed, although at 
first they could not be distinguished from the rest of the clump. P. armatus also laid eggs 
that were distinctly faulty at first glance: they assumed neither the spherical shape nor 
the opaque white appearance of freshly laid eggs and were often deposited in amorphous 
masses. The females seemed unable to discriminate between such faulty eggs and healthy 
young eggs, since both were ingested. On the other hand, both types of eggs often 
remained untouched until they either hatched or deteriorated. 
Thus egg cannibalism affected only young eggs, but was otherwise erratic and 
indiscriminate. Lack of a required nutritional component in thc diet may have been the 
cause for both the cannibalistic behaviour and the production of faulty eggs in P. 
armatus. However, no food substances other than yeast were used in the investigation. 
EGG VIABILITY 
Aside from cannibalistic attack by the fcmales, eggs of P. arrmtus were also found to 
be susceptible to excessive fungal and bacterial contamination. Fungal growth was 
particulaly heavy at 26"C, in spite of constant efforts to keep the jars clean. Many egg 
clunlps were therefore not suited for precise counts of egg viability, including those 
which had been only partially ingested or were partly overgrown by fungi. 
At each temperature over-all data on hatching success were finally derived from egg 
clumps which showed no fungal infection and had not been attacked by the parent. Eggs 
laid at 15°C had a higher percentage of viability than those laid a t  21' and 26°C (Table 
5
Snider: The Life Cycle Relative to Temperature of Protaphorura Armatus (T
Published by ValpoScholar, 1974
14 THE GREAT LAKES ENTOMOLOGIST Vol. 7,  No. 1 
Table 4. Viability of e g s  of l+otaphorura armatus at  three temperatures. 
No. of eggs 1216 1062 8 84 
No. hatched 949 719 567 
Percent 78.0 67.7 64.1 
4). At least under laboratory conditions, large clump size and high egg viability may 
possibly compensate for the low percentage of females reproducing at lS°C. 
The over-all viability figures given in Table 4 are probably an overestimate, since data 
on faulty eggs were treated separately. At 26"C, 4.5Y of all eggs laid were faulty and 
clearly non-viable, as compared to 3.1% at 21°C and 3.5% at 15°C. 
SUMMARY 
Laboratory observations on  Protaphorura armatus (Tullberg) disclosed parthenogenetic 
reproduction in the species. Males have as yet not been found in either the stock cultures 
or among specimens collected from Michigan soil samples. 
Isolated individuals of P. armatus were reared at 15', 21' and 26°C. Longevity and 
survival were greatly extended at  lS°C, at which temperature the duration of the stadia 
was longest. Eggs were laid in clumps within a few days of ecdysis. The largest clumps 
were recorded at  ISo, but  at  that temperature a lower percentage of females laid eggs 
than at  21' or 26°C. Eggcannibalism occurred frequently and affected both healthy and 
faulty young eggs. 
ACKNOWLEDGMENTS 
I am indebted to Dr. Richard J. Snider for criticism and encouragement, and to Dr. 
James W. Butcher for providing the necessary facilities for this study, which was carried 
out under the Department of Entomology Soil Biology Program at  Michigan State 
University. 
LITERATURE CITED 
Choudhuri, D. K. 1958. On two new species of Onychiurus Gervais (Collembola: 
Onychiuridae) froin the British Isles. Proc. R. Entomol. Soc. London (B) 27:155-159. 
Green, C. D. 1964. The effect of crowding upon the fecundity of Folsonlia candida 
(William) var. distincta (Bagnall) (Collembola). Entomol. Exp. e t  Appl. 7:62-70. 
Hale, W. G. 1964. Experimental studies on  the taxonomic status of some members of the 
Onychiurus armatus species group. Rev. Ecol. Biol. Sol 1(3):501-510. 
Hale, W. G. 1965. Observations on the breeding biology of Collembola. Pedobiologia 
5:146-152, 161-177. 
Hale, W. G. 1966. The Collembola of the Moore House National Nature Reserve, 
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Huther, W. 1961. Oekologische Untersuchungen uber die 1:auna ppdlzischer Wein- 
bergsboden. Zool. Jahrb. Syst. 89:243-368. 
Marshall, V. G. and Kevan, D. K. McE. 1962. Preliminary observations o n  the biology of 
Folsomia candida Willem, 1902 (Collembola: Isotomidae). Can. Entomol. 94575-586.  
Mayer, H. 1957. Zur Biologie und Ethologie einheimischcr Collembolen. Zool. Jahrb. 
Syst. 85:501-570. 
Petersen, H. 1965. The Collembola of the Hansted Reserve, Thy, North Jutland. 
Taxonomy, Ecology. Entomol. Medd. 30: 3 13-395. 
Petersen, H. 1971. Parthenogenesis in two common species of Collembola: Tullhrrgia 
krausbaueri (Borner) and Isotoma rzotabilis Schaffer. Rev. Ecol. Biol. Sol 
8(1):133-138. 
Schaller, 1:. 1953. Untersuchungen zur Fortpflanzungsbiologje Arthropleoner Col- 
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The Great Lakes Entomologist, Vol. 7, No. 1 [1974], Art. 3
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1974 THE GREAT LAKES ENTOMOLOGIST 15 
Snider, R. M. 1973. Laboratory observatior~s on the biology of Folsornia ca~zdida 
(Willem) (Collembola: Isotomidae). Rev. Ecol. Biol. Sol 10(1):103-124. 
Vail, P. V. 1965. Colonization of Hypogastrura rnarzubrialis (Collembola: Poduridae) with 
notes on its biology. Ann. Entornol. Soc. Amcr. 58(4):555-561. 
Waldorf, E. S. 1971a. The reproductive biology of Sinella curviseta (Collembola: 
Entomobryidae) in laboratory culture. Rev. Ecol. Biol. Sol 8(3):451-463. 
Waldorf, E. S. 1971b. Selective egg cannibalism in Sinella curvlseta (Collernbola: 
Entomobryidae). Ecology 52(4):673-675. 
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Snider: The Life Cycle Relative to Temperature of Protaphorura Armatus (T
Published by ValpoScholar, 1974


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The Life Cycle Relative to Temperature of Protaphorura Armatus (Tullberg) (Collembola: Onychiuridae), a Parathenogenetic Species

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