in Victoria. Catherine Yule. Department of Zoology, Monash University, ... the species were univoltine (except for D, eucumbene, which had a nymphal life span ...
Aust. J. Mar. Freshw. Res., 1985, 36, 717-35
Comparative Study of the Life Cycles of Six Species of Dinotoperla (Plecoptera :Gripopterygidae) in Victoria
Catherine Yule Department of Zoology, Monash University, Clayton, Vic. 3168. Present address: Department of Applied Biology, Royal Melbourne Institute of Technology, G.P.O. Box 2476V. Melbourne, Vic. 3001.
Abstract
The life cycles of six species of Dinotoperla were studied. One of these, D. bassae, only occurred in temporary pools; three species, D. thwaitesi,D. fontana and D. brevipennis,were found in intermittently flowing creeks; and these three species as well as D. eucumbene and D. christinae inhabited cool, permanent rivers. All the species were univoltine (except for D, eucumbene, which had a nymphal life span of 11-15 months). D. bassae, D. brevipennis,D. christinae and D. eucumbene had seasonal well-synchronizedlife cycles, although in times of severe drought the eggs of D. bassae may remain in diapause for 18 months or more. Emergence periods of all species were relatively restricted and were completed by early summer.
Introduction
The life cycles of the stoneflies in the Southern Hemisphere are very poorly known when compared with the wealth of data accumulated for Northern Hemisphere species over the past 50 years (e.g. Hynes 1941; Brinck 1949; Harper 1973a, 1973b; Mutch and Pritchard 1982; Folsom and Manuel 1983; Lechleitner and Kondratieff 1983).In New Zealand, Winterbourn (1966, 1974) has investigated aspects of the life histories of species in all four Southern Hemisphere families (Eustheniidae, Austroperlidae, Notonemouridae, Gripopterygidae); however, there have been few studies of the life cycles of Australian Plecoptera (Hynes 1964; Hynes and Hynes 1975; Marchant et al. 1984). Hynes and Hynes (1975) outlined the life cycles of 34 Victorian species (including five species of Dinotoperla) from the four Australian families. They noted that, in comparison with Northern Hemisphere species, Australian stoneflies tend to have very flexible life cycles with great variation in the periods of egg diapause, hatching, growth and emergence, which they attributed to the uncertainty and aridity of the Australian climate. Flexibility may be an inherent character of many stonefly life histories as it has frequently been reported for Northern Hemisphere species also. A decrease in nymphal growth rates, resulting in later emergence of adults, related to an increase in altitude and latitude (and hence to a decrease in temperature) occurs in many European Plecoptera (e.g. Brinck 1949; Hynes 1970; Radford and Hartland-Rowe 1971; Cather and Gaufin 1975). Prolonged emergence periods are also common in the Northern Hemisphere (Kerst and Anderson 1974). To investigate further the variability of the life cycles of Australian Plecoptera, the life histories of six Victorian species of Dinotoperla were compared. Species of 0067-19401851050717$02.00
Catherine Yule
Dinotoperla occur in a wider range of freshwater habitats than do those of any other Australian genus so far studied. They have been recorded from lakes (in Tasmania), mountain streams, lowland rivers and even temporary pools and drains (Hynes 1982). Hynes and Hynes (1975) described the life cycles of Dinotoperla 'arenaria' ( = D. eucumbene),D. christinae, D. brevipennis and a species later recognized as D. fontana (the adults of which were confused with D. serricauda-see Yule 1984). They also outlined the life cycle of a species that they called D. 'serricauda', but this may have been D. thwaitesi or else may have included both species. Where possible, Hynes and Hynes' results have been used to supplement the data obtained in this study. The life cycle of D. bassae (and possibly D. thwaitesi) has not previously been examined. Since D. bassae is the only stonefly known to inhabit temporary lentic habitats in Australia, the life history of this species is of particular interest. Table 1. Summary of the physical characteristics of the sampling sites in the Otway Ranges and at Daylesford
Site
Altitude (m.a.s.1.)
Water temp. ("(2) Min. Max.
RainfallA
(m-4
Flow rateB (M1 day- ') Min. Max.
Sailors Creek
600
5.8
17
890
-
-
Wombat Creek
502
7
20
890
-
-
Jim Crow Creek
420
8.2
19.5
890
0.7
125
Aire River
267
9
15
1751
14.2
163
73
8
16.5
1082
11 .8
185
Lardners Creek
Substrate
Large boulders and cobbles on coarse sand Boulders and cobbles on fine to coarse sand Boulders and cobbles on gravel and coarse sand Boulders, cobbles, gravel, sand and silt Fine to coarse sand and silt with occasional boulders
A Data from Commonwealth Bureau of Meteorology gauging stations. Daylesford was the closest station to Sailors Creek, Wombat Creek and Jim Crow Creek. Data from State Rivers and Water Supply Commission (1979-1980). Sailors Creek and Wombat Creek unite to form Jim Crow Creek.
Study Sites
Sampling sites were selected on the basis of four main criteria: the presence of large populations of species of Dinotoperla, a range of altitudes and flow rates between the sites, and accessibility. Two sites were chosen in the Otway Ranges-Lardners Creek (38"32'S.,143"33'E.) and the Aire River (38"40rS.,143"36'E.), and three sites near Daylesford-Sailors Creek (37"24'S.,l44"8'E.),Wombat Creek (37"21'S.,l44"8'E.)and Jim Crow Creek (37"17'S.,l44"7'E.).For the study of D. bassae, two temporary pools named in this study Pomborneit Pond (38"11'S.,143"20'E.) and Ibis Pond (38°13rS.,143019rE.) were selected in the Stony Rises near Lake Corangamite. The three creeks sampled in the Daylesford area are all part of the same catchment system. They frequently cease flowing in summer, becoming a series of pools. The Aire River and Lardners Creek are permanent streams in discrete coastal catchments. The
Life Cycles of Dinotoperla
physical characteristics of the sites are summarized in Table 1. Riparian vegetation along the rivers typically consists of eucalypts ( e g Eucalyptus radiata Sieber ex DC., E. obliqua L'HCrit. and E. viminalis Labill.) and wattles (e.g.Acacia melanoxylon R. Br.) with a ground cover of exotic weeds and native herbs. The temporary pools recurrently occurred in the Stony Rises, which are a maze of ridges, troughs and basins formed by geologically Recent lava flows (Sherbon-Hills 1967). They filled with water (in June 1979 and in April 1980) due to surface runoff and a rise in the water table. They dried up over the summer months and were usually completely dry by February. The aquatic flora was composed of native species (e.g. Myriophyllum propinquum A. Cunn., Potamogeton tricarinatus F. Muell. et A. Bennett ex A. Bennett, Juncus pallidus R. Br., Scirpus fluitans L. and Chara sp.) whereas the riparian species were almost all exotic (e.g. Phalaris minor Retz., Holcus lanatus L.). The maximum dimensions recorded for Pomborneit Pond were 30 by 32 m and a depth of 1.25 m in August 1980; Ibis Pond reached a size of 10 by 4 m and a depth of 0 . 6 m. The mean total rainfall in the region (Colac) was 721 mm.
Methods The fauna of the creeks was sampled monthly for a minimum of 12 months and the temporary ponds were sampled weekly or fortnightly when water was present. The creeks and rivers were sampled qualitatively using a hand-held plankton net 22 by 24 cm, with a mesh size of 0.45 mm. The mesh size was chosen after investigation of the size of first-instar nymphs. The body lengths of Dinotoperla nymphs hatched from eggs by Professor H. B. N. Hynes (specimens in the Museum of Victoria) were all greater than 0.5 mm. It was not realized until later that the diagonal measurement of the mesh (0.53 mm) was too large to trap all the first-instar nymphs, so on several occasions supplementary samples were taken at each site with a handheld plankton net of 0.175-mm mesh. This net was used for all samples from the temporary ponds. At each site, two 4-min kick samples, each covering several square metres, were taken. The samples were preserved in Kahle's solution. Adults were collected by means of a net swept through the riparian vegetation and by handpicking from vegetation and rocks and also below bridges. They were preserved in 70% ethanol. In order to determine growth rates of nymphs and synchrony of their development, up to 50 nymphs of each species were measured each month (more frequently for D. bassae). Larger nymphs were sexed, males being recognized by a point on the last abdominal segment, which developed into a hook in the final instar. Very small, early-instar nymphs were measured to the nearest 0.0125 mm and larger nymphs were measured to the nearest 0.025 mm using an ocular micrometer of 0,025-mm un~tsat a magnification of 80 x . For each nymph, head width, total length and mesonotum width ( =wing-pad width) and length (=wing-pad length) were measured to evaluate the reliability of each body part as an index of growth. Total body length proved unsatisfactory despite its common usage (e.g. Hynes 1941; Brinck 1949; Minshall and Minshall 1966; Clifford 1969; Barton 1980) because telescoping of thoracic and abdominal segments caused considerable variations in size. Head width has been the most frequently used body part as an index of growth in plecopteran life-history studies (e.g. Holdsworth 1941a, 1941b; Tarter and Krumholz 1971; Sheldon 1972; Harper 1973a, 1973b; Winterbourn 1974; Cather and Gaufin 1975; Hynes and Hynes 1975; Mutch and Pritchard 1982; Lechleitner and Kondratieff 1983),but it is not necessarily the most reliable parameter (Yule 1982).Differences in wing-pad length were related to variations in wing-pad development (i.e. wing-pad shape) and laboratory observations of nymphs confirmed that these changes in wind-pad development corresponded to different instars. However, nymphs in different instars frequently had the same head width (and also wing-pad width). Head width and wing-pad length were closely correlated but the rate of increase in the size of the wing pads was greater than that of the head. Thus, the use of wing-pad lengths results in greater gaps between later instars, allowing clearer determination of development rates. Sexual dimorphism in size was also investigated based on the wing-pad lengths of nymphs and forewing lengths of adults, t-Tests (unmatched pairs) were performed. Probability values obtained from the t-test were considered highly significant (0.05 > P > 0.001) and very highly significant (P < 0.001). Sex ratios were also determined for each species.
Catherine Yule
Results The length of time given for each stage in the life history is based upon the data collected in this investigation and also, where applicable, on information from Hynes and Hynes (1975). Specimens in the Museum of Victoria collection provided additional information on adult flight periods. The incubation period of the eggs is the time elapsing from the laying of the egg mass to the hatching of the eggs. Where it is lengthy, it indicates either an egg diapause or else very slow embryonic development. The length of the incubation period was inferred from the time between the adult flight periods and the re-appearance of small nymphs. The life cycles of each of the six species of Dinotoperla in this study are presented below and summarized in Table 2. Table 2.
Species
D. eucumbene
Summary of life-cycle characteristics of Dinotoperla species
Incubation period of eggs
Timing of nymphal recruitment
D. fontana
Absent or else Synchronous, 9-12 months Aug.-Oct. 8-10 months Usually synchronous, April-July 6-9 months Extended, June-Sept. 0-4 months Synchronous, Oct. Very flexible Extended
D. thwaitesi
Very flexible
D. bassae
D. brevipennis D. christinae
Period of nymphal development 11-15 months 2 k 4 months (winter-spring) 4-5 months (winter) 9 months
6 months? (mostly winter) Extended but mostly 6 months? April-May Absent in late summer (early autumn)
Timing of adult emergence
Adult flight period
Synchronous, Aug..-Nov. Aug.-Sept. Synchronous, Aug.-Nov. Aug.-Oct. Synchronous, Nov.-Feb. Nov. Synchronous, July-Nov.? July-Aug.? Extended, Sept.-Jan. winter-spring Extended, July-Jan. winter-spring
Dinotoperla eucumbene McLellan D. eucumbene was common at Lardners Creek and was also found at the Aire River. This species has a clearly defined, regular life cycle with a well-synchronized pattern of development (Figs 1 and 2). The life cycles at the two sites were very similar. In 1980, newly hatched nymphs were first collected from both sites in August. In 1979, they were not found in Lardners Creek until October. The rate of nymphal growth was quite uniform; however, mortality appeared high as few later-instar nymphs were found. In Lardners Creek, final instars occurred in July and August. In the Aire River, they were most common in August with one specimen being collected in September. From Figs 1 and 2, the minimum time taken from hatching to emergence at these sites would be 10 months (October to July) and the maximum would be 14 months (August to September of the next year). Adults were found in September at both sites. Hynes and Hynes (1975)studied the life cycles of this species in Crown Creek, Wilks Creek and the Delatite River in Victoria. Their results indicate a somewhat longer period of nymphal growth (up to 15 months) with eggs hatching possibly as early as May. Final-instar nymphs were present between July and September in the warmer streams and between August and October in the cooler Delatite River. The adult flight period at Wilks Creek and Crown Creek lasted from September to October but no adults were
Life Cycles of Dinotoperla
found at the Delatite River although Hynes and Hynes collected one mature female in February high up on Mount Buller (where the low temperatures probably retarded emergence). Fig. 1
2.25 -
1 8.7 9 adults .
,
10 H
N=514
61 9
2.00 . 1.75
0
1 M
A
M
J
J
0
A
N
D
J
F
Fig. 2
M
A
J
J
A
S
O
N
D
36.1 P adults
0
1 F
M
A
M
J
J
A
S
O
N
D
1980
Figs 1 and 2. Temporal variation in wing-pad size frequency distribution for D. eucumbene in Lardners Creek (I)and in the Aire River ( 2 ) .In these and the following figures, except Fig. 17, the total number of nymphs examined and the number and sex of adults collected are indicated.
Although the eggs appeared to hatch more or less in synchrony at all sites, their development may follow one of two strategies. The eggs might be laid very soon after adult emergence and hatch immediately, but more probably the females oviposit a month
Catherine Yule
or so after emergence (since the females, and their eggs, are not mature on emergence) and the eggs lie in diapause (or undergo very slow development) until the following winter. Depending on the life span of the adults (which appears to be 1 or 2 months), the eggs could lie in diapause for 8-12 months. Both strategies of egg development may occur. Males (both adults and final-instar nymphs) were highly significantly smaller than females, with the females (last-instar nymphs) outnumbering males by 1 . 8 to 1 (N = 18). Dinotoperla christinae McLellan This uncommon species was found at Lardners Creek and the Aire River. A total of 232 nymphs was collected from Lardners Creek but too few specimens were obtained from the Aire River for nymphal growth to be analysed at this site.
o
,
,
A
M
, J
,
J
A
S
1979
-
,
O
r
N
D
J
7
7-
F
M
A
M
J
J
A
S
O
N
D
1980
Fig. 3. Temporal variation in wing-pad size frequency distribution for D. christinae in Lardners Creek.
In 1979 and 1980, small nymphs first appeared in Lardners Creek in late October, indicating that hatching of the eggs occurred earlier in the month (Fig. 3). A fairly uniform rate of nymphal growth resulted in final instars occurring in July 1979. No final-instar nymphs were collected in 1980 but the specimens found in June were in their penultimate instar so emergence probably did not occur until July. In the Aire River, one nymph in its final instar was collected in July 1980. Mortality of the nymphs was very high as their numbers decreased greatly with increasing size. Adults were never found although Hynes and Hynes (1975) collected one mature female at the Aire River on 9 November 197 1. Therefore, although first-instar nymphs were not found, the life cycle at Lardners Creek is quite clear. Adults probably live for several months, ovipositing in September or October. The eggs presumably develop rapidly and hatch soon after being laid. Judging from the monthly size distribution data, hatching is synchronous, with emergence taking place approximately 10 months later. A small population of D. christinae in the Aberfeldy River was studied by Hynes and Hynes (1975). The development of nymphs in this population was not entirely synchronous as several final-instar nymphs were found in March, June, August and
Life
Cycles
723
of Dinotoperla
September. However, the general life-cycle trend was similar to that seen in Lardners Creek, with nymphal growth during autumn and winter and emergence in late winter and early spring. Insufficient specimens were present to examine sexual dimorphism in size or to determine sex ratios. Dinotoperla brevipennis Kimmins D. brevipennis was common in Lardners Creek and nymphs were also collected in small numbers from Sailors Creek, Wombat Creek and the Aire River. Nymphs were only present in winter and early spring. The rate of nymphal growth was very rapid (Fig. 4). Nymphs were found in Lardners Creek between June and October in 1979 and 1980, indicating a possible maximum growth period of 5 months. In 1979, very small nymphs were collected from June until September, showing that nymphal recruitment lacked synchrony. Final-instar nymphs were collected in September 1979 and October 1980. The adult flight period was quite long, occurring from November through to February in Lardners Creek. A single adult male was collected at Sailors Creek in November 1979.
75p01
48.69 19
-E E
6 8.7 9 adults
19
I
1.50
1.25.
U l
,
M
Fig. 4.
J
J
A
Temporal variation
S
O
N
D
J
F
M
A
M
J
J
A
S
O
N
D
in wing-pad size frequency distribution for D. brevipennis in Lardners Creek.
The life cycle of D. brevipennis in Lardners Creek is well defined. There is an egg diapause of up to 8 months over summer and autumn, with the nymphs hatching out in winter and developing rapidly to emerge in spring. Diapause in the eggs of D. brevipennis was investigated by Hynes (1974).Eggs incubated in the laboratory produced hatchlings from May until October. Although sexual dimorphism in size was insignificant in final-instar nymphs (possibly due to small sample sizes), the larger size of adult females than adult males was very highly significant. The sex ratio of final-instar nymphs was Id : 1.289 (N = 11). Dinotoperla fontana Kimmins This was the only species to occur at all of the study sites in the Otway Ranges and in the Daylesford area. It was most abundant in the Aire River and Wombat Creek.
Catherine Yule
adults
1980 Fig. 6
Fig. 7 2.25 2.00
a
,
,
,
2,329
19
2$,2Padults
18.19
-
-
5
0
13
0
0,
,
.
J
F
M
I I I I
M
J
J
A
S
O
N
D
,
A
,
M
,
J
0 ,
J
A
S
O
N
D
Life Cycles
725
of Dinotoperla
Recruitment of young nymphs occurred at all sites throughout the year except during late summer and early autumn (Figs 5-9) but final-instar nymphs were only found between June and December (except for one specimen from the Aire River in February). Fig. 8
2.00
-
1
p
1.25-
5
adults
&I
d c $1
4 I
1
0
3
0
0
1
3
0
C
-
1.3
10 N=450
4
1.001
m
18
-
1.75 !
-0
28.29
19
by
2.25-
0
0.75.
I
0
0
0
0
0
0
1
0501 I
n
0
D
B
o
, M
, J
, J
, A
, S
, O
, N
, D
J
.----,
,
,
,
,
,
F
M
A
M
J
Fig. 9
J
A
S
"
,
,
,
O
N
D
19 adult
J
F
M
A
M
J
J
A
S
O
N
D
Temporal variation in wing-pad size frequency distribution for D ,fontana in the Aire River ( 5 ) , in Lardners Creek ( 6 ) ,in Sailors Creek ( 7 ) , in Wombat Creek (8) and in Jim Crow Creek ( 9 ) .
Figs 5-9.
Adults were present between September and December. Neither final instars nor adults were found at Lardners Creek even though large numbers of small nymphs were collected here. The mortality rate appeared particularly high at this site; however, it is possible that the nymphs moved to an unsampled habitat, such as deep down in the substrate.
Catherine Yule
Hynes and Hynes (1975) described the life cycle of D. fontana under the name Dinotoperla sp, as they had confused the adults of this species with D. 'serricauda' (Yule 1984). They found few final instars of this species: several in November in the Grampians, two in October in the East Tanjil River, and one in Crown Creek in March.
o
e
0250
M
J
J
A
S
O
N
D'
J
F
M
A
M
J
J
A
S
O
N
D
1980
Figs 10 and 11. Temporal variation in wing-pad size frequency distribution for D. thwaitesi in Sailors Creek (10) and in Wombat Creek (11).
Of 32 adults examined in the Museum of Victoria, all had been collected between September and January except for two mature females that had been caught in February and early March.
Life Cycles of Dinotoperla
There is probably a very flexible period of egg diapause in this species as hatching of eggs apparently occurs throughout most of the year. Although small nymphs are present in early summer, few of these appear to survive to their final instar and it is even rarer for them to emerge as adults. (It is possible, however, that there is a nymphal Fig
12
J
2a
1Q
F
M
A
M
J
J
A
S
O
N
adults
D
IS80 Fig. 13
78.29
28.2 9
adults
I
=
:
; eo e $ c i 3
rn
D
~
+o F
M
A
M
J
J
A
S
O
N
D
Figs 12 and 13. Temporal variation in wing-pad size frequency distribution for D. thwaitesi in Jim Crow Creek (12) and in the Aire River (13).
diapause in the hotter months of the year.) The length of nymphal development is variable but probably takes about 6 months with most eggs hatching in late autumn and early winter, culminating in emergence in early summer. Female nymphs in their final instar were highly significantly larger than males and they outnumbered males by 1 21 to 1 (N = 7 1).
Catherine Yule
Dinotoperla thwaitesi Kimmins This common species was collected in large numbers from the three Daylesford sites and the Aire River. It had a life cycle very similar to that of D. fontana with which it was frequently found throughout Victoria (see Yule 1984). Small nymphs were present throughout the year except for late summer and early autumn (Figs 10-13). D. thwaitesi nymphs were absent from all sites in March and from several sites in January and February (when water temperatures were high). Early instars were most prolific in April and May. The adults and final instars were more numerous than those of D. fontana and they occurred over a longer period of time. Final instars were found from July through to January and one specimen was collected from the Aire River in April. Adults were found between July and December. All of the 7 1 specimens examined in the Museum of Victoria had been collected between July and January except for a male and a female collected in the Snowy Mountains (N.S.W.) in February and a mature female collected in Victoria in March. The life cycle of most specimens appeared to exhibit the following pattern: an egg diapause over summer with hatching late in autumn, nymphal growth through winter and emergence as adults in spring. Sexual dimorphism in size was very highly significant in both final-instar nymphs and adults, with the mean forewing length of females being 1 . 1 mm longer than that of males. The sex ratios were l d : 1.179 (N = 294). Dinotoperla bassae Hynes Nymphs of this species inhabited pools and drains that dried up in summer. Firstinstar nymphs hatched out (together with microcrustacea and macrocrustacea such as notostracans) within days of the initial formation of the pools in spring or winter. In 1979, Pomborneit Pond began to fill with water in June but in 1980 it started to fill in April; inundation of Ibis Pond did not commence until July. Following a severe drought in 1982 when the ponds remained dry, D. bassae nymphs re-appeared in the winter of 1983 when the ponds filled again. Thus, the eggs had remained in the dry mud for more than 18 months before hatching. Development of the nymphs, although slightly variable in timing, was extremely rapid (Figs 14-16). Final-instar nymphs were initially collected from Ibis Pond in late August, 2 months after the first appearance of nymphs, and adults were collected 2 weeks later, a total of 21 months from hatching to emergence (Fig. 16). Nymphal development in Pomborneit Pond was slower, taking about 3 months to reach the final instar in 1979 and 1980. In 1979, adults were first found 2 weeks after final-instar specimens were initially collected but in 1980 they did not appear until 1 month afterwards (a total of 4 months from hatching till emergence). This variability in timing of hatching and emergence is reflected in the sizes attained by final-instar nymphs. In 1980, nymphs from Pomborneit Pond were significantly larger than those from Ibis Pond, which hatched 2 months later. Emergence from Pomborneit Pond commenced 2 weeks earlier, hence the nymphal growth period was 6 weeks longer than in Ibis Pond. Similarly, final-instar nymphs from Pomborneit Pond were significantly larger in 1980 than in 1979 when nymphal development time was 2 weeks shorter. The adult flight periods varied in length from 1 month at Ibis Pond to 2 months at a nearby pond. Adults were rarely seen flying and were always found close to the pools. In 1979 and 1980 at Pomborneit Pond, adults were found over a 6-week period.
Life Cycles of Dinotoperla
The earliest appearance of adults was late August in 1980 (at Pomborneit Pond) and they were found up until the end of November in 1979. There was a tendency towards a decrease in size of later emerging adults (each sex considered separately) but this was Fig. 14 2.25
Fig. 1 5
Figs 14 and 15. Temporal variation in wing-pad size frequency distribution for D. bassae in Pomborneit
Pond in 1979 (14) and in 1980 (15).
Catherine Yule
158,139 36a.389j 59
adults
" 1 , 19.vi 3.vii
14.vii
3l.vii
Zl.viii28.viii
, 1 26.ixl.xlO.x 27.x
12.ix
1980 Fig. 16. Temporal variation in wing-pad size frequency distribution for D. bassae in Ibis
Pond in 1980.
o l A
,
,
,
,
,
M
J
J
A
S
Winter
1979
, O
, N
, D
, J
Summer
,
,
,
F
M
A
M
J
J
A
S
O
N
D
Winter
1980
D. eucumbene (- - - - -), D. Fig. 17. Sequential emergence of D. christinae (-), brevipennis (-.-.-.-) and D. fontana (. . . . . . .) at Lardners Creek. Arrows indicate emergence of adults.
Life Cycles of Dinotoperla
73 1
not always consistent. At all sites the males tended to emerge slightly earlier than the females; however, the females were still found for about a fortnight after the last males were seen. It seems that males can emerge before females due to more rapid development but this is at the expense of achieving equal size. The final-instar female nymphs (and adults) were highly or very highly significantly larger than male nymphs in each population studied. This sexual dimorphism in size was also significant for second-last instar specimens but not for those in the preceding instar. This indicates that the rate of growth and development of male and female nymphs is initially synchronous. Among the 47 1 final-instar nymphs measured, females outnumbered males by 1 .24 to 1. Sequential Emergence Sequential emergence of adults occurred in Lardners Creek (Fig. 17). Adult D. christinae were not found but the presence of final instars in late June indicated that emergence occurred in July, adults of D. eucumbene first appeared in September, and those of D. brevipennis were not found until November. Although neither final instars nor adults of D. fontana were collected, growth-rate data indicate that emergence occurred in mid-summer; however, the life cycle of this species is generally quite flexible. As can be seen in Fig. 17, whenever nymphs of different species were found together, they were usually in different size classes (except for D. christinae and D. eucumbene nymphs for a short period). Discussion
Except for Antarctica, Australia has the lowest average annual rainfall of any continent (Bayly and Williams 1973). This lack of water is compounded by the fact that Australia also has the highest percentage evaporation and lowest percentage runoff (Williams 1980).Furthermore, the discharge of streams in Australia, even those of the south-east, is markedly more variable than elsewhere in the world (Lake et al. 1985). Since most of the Australian continent is subject to such an arid and uncertain climate, the life cycles of many of the aquatic insects of Australia are characterized by their flexibility. For example, well-synchronized life histories have been found in only three of eleven species studied from the La Trobe River (Marchant et al. 1984) and two of eleven species of Ephemeroptera examined by Duncan (1972) and Campbell (1983). When Hynes and Hynes (1975)investigated the life histories of 34 species of Plecoptera in Victoria, they concluded that, in general, because of the unpredictable climate, they had less-rigid life cycles than species in the Northern Hemisphere. However, in the present study, four of the six species of Dinotoperla observed (D. eucumbene, D. bassae, D. brevipennis and D. christinae) had well-synchronized, seasonal life cycles. In general, the timings of egg diapause, hatching, growth and emergence appeared to be no more variable than those recorded for many European and North American species (particularly where studies have been undertaken over more than one generation at several different sites). Further, the distribution of species of Dinotoperla, and indeed most Australian stoneflies, is restricted to the less uncertain temperate south-eastern region of Australia (Tasmania,Victoria and eastern New South Wales). For instance, the average annual rainfall at Beechforest (near the Aire River and Lardners Creek) was more than four times higher than the average annual rainfall for the whole of Australia, and at Daylesford the average annual rainfall was over twice that of the entire continent. Possibly more importantly, the streams in this study were relatively cool, the highest temperature recorded being 20°C at Wombat Creek. As
Catherine Yule
pointed out by Lake et al. (1984),synchronous life histories appear to be common in the cooler waters of south-east Australia and at the higher latitudes of the Northern Hemisphere. The permanent flow and small temperature ranges (Table 1) of the Otway streams enabled nymphs of D. eucumbene and D. christinae to grow throughout summer, which is generally a very harsh season for the Australian aquatic fauna. D. brevipennis nymphs completed their development in winter but they had an extended period of nymphal recruitment due to an egg diapause of flexible duration. This diapause was apparently an adaptation to the less-predictable habitats (in terms of discharge) in which this species occasionally occurred. Despite their name, the temporary pools inhabited by D. bassae were in fact relatively predictable environments. Inundation of the pools, although somewhat variable in timing, was an annual, winter event, and, with the advent of spring, they were filled to such a depth as to prevent large diurnal fluctuations in water temperature. Hatching of D. bassae nymphs commenced as soon as the pools started to fill with water in winter when temperatures were low, and emergence occurred in spring before conditions became adverse to growth with higher water temperatures, decreased oxygen levels and final disappearance of the pools in summer. Hence, nymphal development and adult emergence were usually highly synchronized in populations of this species. In years of very severe drought, however, the temporary pools may remain dry throughout winter, in which case the eggs appear to remain in diapause until the following winter. The life histories of D. fontana and D. thwaitesi, on the other hand, were very flexible. Nymphs of all sizes were found during most months of the year, although seasonality of growth was exhibited by large proportions of their populations so that emergence was mostly confined to late spring and early summer. These species inhabited creeks that ceased flowing in summer and, consequently, were subject to greater temperature fluctuations than the permanent streams in the Otways. In comparison with other Victorian stoneflies (studied by Hynes and Hynes 1975), D. bassae, D. brevipennis, D. thwaitesi and D. fontana had very short periods of nymphal development. This could be explained by the ephemeral nature of the habitats in which they often occurred (temporary pools and intermittently flowing creeks). Of the species studied by Hynes and Hynes (1975),the eustheniids and austroperlids spent up to 4 years as nymphs and the nymphal development of other gripopterygids (e.g. species of Riekoperla, Leptoperla and Trinotoperla) generally lasted a year or more. The life cycles of the four notonemourid species investigated by Hynes and Hynes (1975) were not clearly defined but mostly the nymphal life span was about 1 year, although possibly Austrocercella ( = Spaniocerca) tillyardi had a bivoltine life cycle. The period of nymphal recruitment was extended in all the species except D. eucumbene and D. christinae. The timing of recruitment in D. bassae varied, depending on rainfall patterns and hence the timing of inundation of the pools. In D. brevipennis, very small nymphs were collected from June until September, yet emergence was restricted to November. In fact, there was relatively very little variability in the timing of emergence of any of the species from year to year or between populations at different sites. Various theories have been proposed to explain such short synchronous emergence periods in aquatic insects. In a study on dragonflies, Lutz (1968) discovered that the various successive instars possessed higher temperature optima for growth. He found that rising vernal water temperatures (and also increasing photoperiod) induced a degree of synchrony into moulting and emergence. The development of would-be late emerging
Life Cycles of Dinotoperla
insects may be hastened by rising water temperatures, increasing day length and also decreasing oxygen levels (or a combination of these factors),resulting in earlier emergence (Hynes and Hynes 1975; Snellen and Stewart 1979).Possibly, this explains the unusually large size observed in final-instar D. bassae nymphs from Pomborneit Pond in 1980. The nymphs hatched much earlier than usual, owing to heavy autumn rainfall filling the pond, but their development was retarded, possibly by low temperatures or short photoperiod. Thus, the nymphs continued to grow until the appropriate environmental cues stimulating metamorphosis and emergence were finally present. By synchronous emergence, all the insects can be released into a favourable environment. Nymphs may be killed by high temperatures or low oxygen levels if they hatch too early or if they are too late metamorphosing into adults (Macan 1958).Adverse conditions quite clearly restrict hatching and emergence in D. bassae. Hynes and Hynes (1975) and also Zwick (198 1) noted a lack of sequential emergence of co-existing Australian species such as has often been reported for Northern Hemisphere species (e.g. Mackay 1969; Radford and Hartland-Rowe 1971; Harper 1973a, 1973b; Kerst and Anderson 1974).However, in this study there was a succession in emergence of D. christinae, D. eucumbene, D. brevipennis and (possibly)D. fontana in Lardners Creek. Temporal succession of adult emergence is one method of habitat partitioning that enables many species to occupy a stream. It can result in reproductive isolation and also allow larval growth periods to be staggered, thus reducing competition for food and space (Kerst and Anderson 1974). The flexibility and lack of seasonality that Hynes and Hynes (1975) believed characterized Australian stonefly life cycles led them to state that it was not possible to assign the species to the 'fast' (embryonic diapause followed by rapid nymphal development)or 'slow' (longer nymphal development with no egg diapause) life-history categories that Hynes (1961, 1970)had devised for Northern Hemisphere aquatic insects. Yet all the species in this study could clearly be classified as fast univoltine species except for D. eucumbene, which had either a slow univoltine life cycle or a semivoltine cycle, and D. christinae, which possibly had a slow univoltine cycle. Nevertheless, such classification schemes tend to be of limited usefulness (except in comparisons of different populations of the same species) because certain species may fall into more than one category depending on environmental conditions. For example, variations in temperature have been shown to influence the timing and duration of adult emergence (Brinck 1949; Harker 1952; Radford and Hartland-Rowe 1971), the rate of nymphal development (Newel1 and Minshall 1978; Vannote and Sweeney 1980), the length of time needed for incubation of the egg (Khoo 1968)and hence the total length of the life cycle. Snellen and Stewart (1979) in the United States discovered that Zealeuctra hitei underwent a univoltine life cycle from non-diapausing eggs in wet seasons, yet had a semivoltine cycle, developing from diapausing eggs, in drought years. Another example of flexibility of life history was reported for Nemoura avicularis by Brittain (1973):this species had a different pattern of growth in Sweden compared with that in Germany and Wales. Flowers and Hilsenhoff (1978) observed the North American mayfly Stenacron tripunctatum had a bivoltine life cycle in Wisconsin although it was apparently multivoltine in Michigan. Thus, contrary to the suggestion of Hynes and Hynes (1975), the life cycles of Australian stoneflies may not differ markedly from many Northern Hemisphere species in terms of timing of egg diapause, hatching, growth and emergence. As for species of the Northern Hemisphere, the flexibility of life cycles exhibited by Dinotoperla
Catherine Yule
eucumbene, D. bassae, D. brevipennis, D. christinae, D. fontana and D. thwaitesi can be related to the predictability of their habitats, particularly in terms of temperature and flow. Since cool freshwater environments are not uncommon in the south-east of Australia (wheremost of the Australian plecopteran fauna is to be found), species with well-synchronized seasonal life cycles should not be considered unusual. This study has highlighted the need for investigations into the life history of a species to be based on more than one generation at more than one site and to be supported with physical data from these habitats. Acknowledgment
I would like to thank Dr P. S. Lake, Monash University, for his helpful advice and criticism. References Barton, D. R. (1980).Observations on the life histories and biology of Ephemeroptera and Plecoptera in north eastern Alberta. Aquat. Insects 2, 97-1 11. Bayly, I. A. E., and Williams, W. D. (1973). 'Inland Waters and their Ecology.' (Longman: Melbourne.) Brinck, P. (1949). Studies on Swedish stoneflies (Plecoptera). Opusc. Entomol. Suppl. 11, 1-250. Brittain, J. E. (1973). The biology and life cycle of Nemoura avicularis Morton (Plecoptera). Freshwater Biol. 3, 199-210. Campbell, I. C. (1983). Studies on the taxonomy and ecology of the Australian Siphlonuridae and Oligoneuriidae (Insecta : Ephemeroptera). Ph.D. Thesis, Monash University. Cather, R. M., and Gaufii, A. R. (1975).Life history and ecology of Megarcys signata (Plecoptera : Perlodidae), Mill Creek, Wasetah Mountains, Utah. Great Basin Nut. 35, 39-48. Clifford, H. (1969). Limnological features of a northern brown-water stream with special reference to the life histories of aquatic insects. Am. Midl. Nut. 82, 578-97. Duncan, M. J. (1972). The life histories of Ephemeroptera from two Victorian streams. BSc. Hons Thesis, Monash University. Flowers, R. W., and Hilsenhoff, W. L. (1978). Life cycles and habitats of Wisconsin Heptageniidae (Ephemeroptera). Hydrobiologia 60, 159-7 1. Folsom, T. C., and Manuel, K. L. (1983). The life cycle of Pteronarcys scotti (Plecoptera : Pteronarcyidae) from the Southern Appalachians, U.S.A. Aquat. Insects 5, 227-32. Harker, J. E. (1952).A study of the life cycles and growth-rates of four species of mayflies. Proc. R. Entomol. Soc. Lond. Ser. A . Gen. Entomol. 27, 77-85. Harper, P. P. (1973~).Life histories of Nemouridae and Leuctridae in southern Ontario (Plecoptera). Hydrobiologia 41(3), 309-56. Harper, P. P. (1973b). Emergence, reproduction, and growth of setipalpian Plecoptera in southern Ontario. Oikos 24, 94-107. Holdsworth, R. P., Jr (1941~).The life history and growth of Pteronarcys proteus, Newman, (Pteronarcydae : Plecoptera). Ann. Entomol. Soc. Am. 34, 495-592. Holdsworth, R. P., Jr (1941b).Additional information and a correction concerning the growth of Pteronarcys proteus, Newman, (Pteronarcydae : Plecoptera). Ann. Entomol. Soc. Am. 34, 714-15. Hynes, H. B. N. (1941).The taxonomy and ecology of British Plecoptera with notes on the adults and eggs. Trans. R. Entomol. Soc. Lond. 91, 459-557. Hynes, H. B. N. (1961).The invertebrate fauna of a Welsh mountain stream. Arch. Hydrobiol. 57, 344-88. Hynes, H. B. N. (1964). Some Australian Plecopteran nymphs. Gewass. Abwass. 34/35, 17-22. Hynes, H. B. N. (1970). 'The Ecology of Running Waters.' (Liverpool University Press.) Hynes, H. B. N. (1974).Observations on the adults and eggs of Australian Plecoptera. Aust. J. Zool. Suppl. 29, 37-52. Hynes, H. B. N. (1982). New and poorly known Gripopterygidae (Plecoptera) from Australia, especially Tasmania. Aust. J. Zool. 30, 115-58. Hynes, H. B. N., and Hynes, M. E. (1975).The life histories of many of the stoneflies (Plecoptera) of southeastern mainland Victoria. Aust. J. Mar. Freshw. Res. 26, 113-53.
Life Cycles of Dinotoperla
Kerst, C. D., and Anderson, N. H. (1974). Emergence patterns of Plecoptera in a stream in Oregon U.S.A. Freshwater Biol. 4, 205-12. Khoo, S. G. (1968). Experimental studies on diapause in stoneflies. I, I1 and 111. Proc. R. Entomol. Soc. Lond. Ser. A. Gen. Entomol. 43, 40-8, 49-56, 141-6. Lake, P. S., Barmuta, L. A,, Boulton, A. J., Campbell, I. C., and St Clair, R. M. (1985). Australian streams and Northern Hemisphere stream ecology: comparisons and problems. Proc. Ecol. Soc. Aust. (In press.) Lechleitner, R. A., and Kondratieff, B. C. (1983). The life history of Pteronarcys dorsata (Say), (Plecoptera : Pteronarcyidae) in south-western Virginia. Can. J. Zool. 61, 1981-5. Lutz, P. E. (1968). Effects of temperature and photoperiod on larval development in Lestes eurinus (Odonata : Lestidae). Ecology 49, 637-44. Macan, T. T. (1958). Causes and effects of short emergence periods in insects. Proc. Int. Assoc. Theor. Appl. Limnol. 13, 845-9. Mackay, R. J. (1969). Aquatic insect communities of a small stream on Mont. St Hilaire, Quebec. J. Fish. Res. Board Can. 26, 1157-83. Marchant, R., Graesser, A,, Metzeling, L., Mitchell, P., Norris, R., and Suter, P. (1984). Life histories of some benthic invertebrates from the La Trobe River, Victoria. Aust. 3. Mar. Freshw. Res. 35,793-806. Minshall, G. W., and Minshall, J. N. (1966).Notes on the life history and ecology of Isoperla clio (Newman) and Isogenus decisus Walker (Plecoptera : Perlodidae). Am. Midl. Nut. 76, 340-50. Mutch, R. A,. and Pritchard, G. (1982).The importance of sampling and sorting techniques on the elucidation of the life cycles of Zapada columbiana (Nemouridae : Plecoptera). Can. 3. Zool. 60, 3394-9. Newell, R. L., and Minshall, G. W. (1978). Life history of a multivoltine mayfly Tricorythodes minutus. An example of the effect of temperature on the life cycle. Ann. Entomol. Soc. A m . 71, 876-81. Radford, D. S., and Hartland-Rowe, R. (1971). Emergence patterns of some Plecoptera in two mountain streams in Alberta. Can. J. Zool. 49, 657-62. Sheldon, A. L. (1972).Comparative ecology of Arcynopteryx and Diura (Plecoptera)in a California stream. Arch. Hydrobiol. 69, 52 1-46. Sherbon-Hills, E. (1967). 'The Physiography of Victoria.' (Whitcombe and Tombs: Melbourne.) Snellen, R. K., and Stewart, K. W. (1979). The life cycle and drumming behaviour of Zealeuctra claasseni (Frison) and Zealeuctra hitei Ricker and Ross (Plecoptera : Leuctridae) in Texas U.S.A. Aquat. Insects 1, 65-89. Tarter, D. C., and Krumholz, L. A. (1971). Life history and ecology of Paragnetina media (Walker) (Insecta : Plecoptera) in Doe Run, Meade County, Kentucky. Am. Midl. Nut. 86, 169-80. Vannote, R. L., and Sweeney, B. W. (1980). Geographic analysis of thermal equilibria: a conceptual model for evaluating the effect of natural and modified thermal regimes on aquatic insect communities. Am. Nut. 115, 667-95. Williams, W. D. (1980). 'Australian Freshwater Life.' 2nd Edn. (Macmillan: Melbourne.) Winterbourn, M. J. (1966).The ecology and life history of Zelandoperla maculata (Hare)and Aucklandobius trivacuatus (Tillyard) (Gripopterygidae). N.Z. 3. Sci. 9, 312-23. Winterboum, M. J. (1974).The life histories, trophic relations and production of Stenoperlaprasina (Plecoptera) and Deleatidium sp. (Ephemeroptera) in a New Zealand river. Freshwater Biol. 4, 507-24. Yule, C. M. (1982).Studies on the biology of Dinotoperla species in Victoria. MSc. Thesis, Monash University. Yule, C. M. (1984).Taxonomic observations on Dinotoperla (Plecoptera : Gripopterygidae) from south-east Australia. Aquat. Insects 6, 201-16. Zwick, P. (1981). Plecoptera. In 'Ecological Biogeography of Australia'. (Ed. A. Keast.) pp. 1171-82. (Junk: The Hague.)
Manuscript received 22 November 1984, accepted 17 April 1985
