Development of larvae of Chrysops nigripes Zetterstedt and Chrysops probably zinzalus Philip (Diptera: Tabanidae) in a subarctic Labrador peatland

Paul E.K. McElligott and David J. Lewis

Abstract: A total of 476 tabanid larvae, including 108 Chrysops nigripes and 145 Chrysops probably zinzalus, were obtained from regular collections made from early June through late August 1990- 1991 in Iron Arm Fen, a minerotrophic peatland located in subarctic Labrador near Schefferville, Quebec. Changes in head capsule and total body length-frequency distributions among successive sampling periods and years suggest very slow growth rates for Chrysops species at subarctic latitudes; life cycles may require 7-8 years to complete.

RCsumC : Au total, 476 larves de tabanides, dont 108 Chrysops nigripes et 145 Chrysops probablement zinzalus, ont CtC rCcoltCes lors d'Cchantillonnages rkguliers effectuks entre le dCbut de juin et la fin d'aoiit, en 1990 et 1991, dans la tourbikre Iron Arm Fen, une tourbikre minkrotrophe situCe dans la zone subarctique du Labrador, prks de Schefferville, QuCbec. Les changements dans les distributions de frkquences des longueurs de capsule cCphalique et des longueurs totales entre les pCriodes d'ichantillonnage et les annCes indiquent que les taux de croissance sont trks lents chez les espkces de Chrysops des latitudes subarctiques; ces insectes peuvent mettre de 7 ii 8 ans ii accomplir tout leur cycle. [Traduit par la RCdaction]

Introduction

Adult female horse flies and deer flies are well known as biting pests of humans and wildlife in subarctic Canada. Most species can be easily collected using a number of types of host-simulating traps. In contrast, their larval stages are seldom encountered, and most aspects of the biology of northern tabanid larvae remain poorly understood (Miller 195 1 ; Teskey 1969; Maire 1984). In particular, the time required for tabanids in northern Canada to complete their life cycle at subarctic latitudes is generally unknown, although Miller (1951) found that tabanid life cycles at Churchill, Manitoba (58 "46'N, 96" 1 1 'W), require a minimum of 3 years. Terterian (1985) reported that certain tabanid species in the former USSR took up to 6 112 years to develop from egg to adult.

The present study examined the length of time required for completion of the life cycles of two deer fly species, Chrysops nigripes Zetterstedt and Chrysops probably zinzalus Philip, in a peatland in subarctic Labrador. It was predicted that their life cycles require a minimum of 3 years for com- pletion, based upon Miller's (1 95 1) findings.

Materials and methods

Quebec (54"49'N, 66"00tW). Eight sampling stations were estab- lished in the fen, selected so as to represent as wide a range as possible of the substrate moisture and vegetation regimes present. Larval Tabanidae and other invertebrates were extracted from sub- strate samples taken at these stations through a combination of wet and dry extraction techniques (McElligott and Lewis 1994). In 1990, samples were collected twice weekly from 14 June to 29 August at four sites. In 1991, twice-weekly sampling from 7 June to 29 August was conducted at eight sites. These sampling periods encompassed, for the most part, those periods in 1990 and 1991 during which the top 10 cm of fen substrate was ice-free (Fig. 1).

The purpose of this study was to determine annual growth patterns of tabanid larvae, and not the presence of distinct instars. Two indicators of growth were therefore measured. In all dipterous larvae body length varies considerably within a given instar, but generally increases as development proceeds. Head capsule length can increase in two ways during larval development: (i) through incremental enlargements with successive larval moults and (ii) within instars through the addition of "growth rings," at least in larval Tipulidae (Pritchard and Hall 1971). In tabanid larvae, head capsule growth appears to be incremental (McElligott 1992). The length of the second antenna1 segment, which has been used to determine instars of Atherix lantha Webb (Diptera: Athericidae) (Lauzon and Harper 1993), was not measured during the present study because it was not possible to obtain the required microscopic resolution under field conditions.

Iron Arm Fen is a 580 x 110 m minerotrophic peatland located in All tabanid larvae collected were either placed in an ice-water subarctic Labrador approximately 20' km northeast of Schefferville, bath until fully extended (Teskey 1969) and measured, or killed

immediately in KAAD, a solution that causes soft-bodied invertebrates Received May 24, 1995. Accepted January 5, 1996. to distend (Martin 1977), and then measured. Each larva's head

P.E.K. McElligott and D.J. Lewis.' Department of Natural capsule length and total body length were measured using a calibrated

Resource Sciences, McGill University (Macdonald Campus), ocular micrometer inserted into the eyepiece of a Wild M5 stereo-

21 11 1 Lakeshore Road, Ste Anne de Bellevue, QC scopic microscope. The head capsule was measured from the anterior

H9X 3V9, Canada. tip of the labium to the posterior bilobed extremity of the epicranium (Fig. 2). Total body length was measured from the anterior tip of ' Author to whom all correspondence should be addressed. the labium on the head capsule to the posteriormost tip of the

Can. J. Zool. 74: 1370- 1375 (1996). Printed in Canada 1 Imprime au Canada

Can

. J. Z

ool.

Dow

nloa

ded

from

ww

w.n

rcre

sear

chpr

ess.

com

by

UN

IV O

F B

IRM

ING

HA

M o

n 11

/09/

14Fo

r pe

rson

al u

se o

nly.

McElligott and Lewis: II

Fig. 1. Mean (f SE) weekly temperatures in the top 10 cm of substrate in Iron Arm Fen, Labrador, during the summers of 1990 and 1991.

-

-

-

-

I I I I . I I 1 I . I I

I June I July 1 August

Fig. 2. Measurement of total body length and head capsule length on a Chrysops larva.

Body Length

Head Capsule Length

extended respiratory siphon (Fig. 2). The body length of very large larvae (> 20 mm) was measured with a millimetre rule rather than the micrometer. Once killed, larvae were preserved in 70% ethanol. Species identifications, where possible, were made using Teskey's (1969, 1983) keys.

Linear regressions of body length against sampling period were calculated using SAS statistical software (SAS Institute Inc. 1985) to determine whether any observed patterns of increase in larval size within size classes were significant.

Results

A total of 406 tabanid larvae were collected during regular sampling at the eight sites in Iron Arm Fen. In addition, 70 larvae were obtained from sporadic collections made at locations in the fen other than the eight study sites (e.g., moss hummocks). For the majority of species (91 1 I), too few larvae (2 -26) were collected to provide sufficient informa- tion for us to draw conclusions concerning seasonal patterns of larval growth (Table 1). Only sample sizes of C. nigripes Zetterstedt and Chrysops probably zinzalus Philip were suffi- ciently large for this purpose. Because of the relatively few

larvae collected on each sampling date, data for 2-week periods were pooled to obtain a succession of length and head capsule frequency distributions over the two summers of study.

Chrysops nigripes One hundred and fourteen C. nigripes larvae were collected during the summers of 1990 and 1991. Length-frequency distributions (Fig. 3a) of these larvae over successive sampling periods indicated the presence of three size categories of larvae co-occurring in the fen. Only three larvae in the smallest category ( 1 4 mm in length) were collected, too few to allow observations concerning their growth rate. In the midlength category, there was an apparent increase in larval size over successive sampling periods, which was significant in 1991 ( p = 0.001, r2 = 0.19) but not in 1990 ( p = 0.067). A two-way analysis of variance (ANOVA) (SAS Institute Inc. 1985), with years and sampling dates as main effects, was carried out to determine if larvae within size categories were, as a group, larger in 1991 than in 1990. This was the case (ANOVA, Fill = 48.49, p < 0.001). Larvae in the midsize category grew very slowly, adding to

Can

. J. Z

ool.

Dow

nloa

ded

from

ww

w.n

rcre

sear

chpr

ess.

com

by

UN

IV O

F B

IRM

ING

HA

M o

n 11

/09/

14Fo

r pe

rson

al u

se o

nly.

Can. J. Zool. Vol. 74, 1996

Table 1. Total numbers of tabanid larvae collected at regularly sampled stations in Iron Arm Fen, Labrador, in 1990 (4 stations) and 1991 (8 stations), and from random sampling conducted elsewhere in the fen in 1991.

1990 1991 Other Total

Chrysops ater Chrysops frigidus Chrysops fircatus Chrysops nigripes Chrysops probably zinzalus Unknown Chrysops sp. Total Chrysopsinae

Hybomitra arpadi Hybomitra epistates Hybomitra itasca Hybomitra pechumani Hybomitra zonalis Unknown Hybomitra sp. Atylotus sphagnicola Total Tabaninae

Total Tabanidae

their length by an average of only 2-3 mm each year, or 4-6 mm over the 2-year study period.

Like larvae in the midsize category, larvae in the largest size category increased in size over successive sampling intervals. This trend was significant in 1991 ( p = 0.035, r2 = 0.15) but not in 1990 ( p = 0.539). Larvae in the largest size category were generally larger in 1991 than in 1990 (ANOVA, Fill = 23.28, p < 0.001).

Successive frequency distributions of head capsule lengths of C. nigripes larvae (Fig. 3B) suggest the presence of at least three distinct cooccurring larval size categories. These distributions appeared to change little with time, in contrast to frequency distributions of body lengths.

Chrysops probably zinzalus Frequency distributions of body lengths and head capsule lengths of 150 larvae of Chrysops probably zinzalus over successive sampling periods (Figs. 4A, 4B) showed trends similar to those found for C. nigripes. Three length categories of larvae were present; there were too few small larvae for conclusions to be drawn regarding their growth. There was a trend of increasing length of midsized larvae over succes- sive sampling periods, which was significant in 1991 ( p < 0.001, r2 = 0.36) but not in 1990 ( p = 0.671). Midsized larvae were generally larger in 199 1 than in 1990 (ANOVA, Fill = 3.59, p = 0.007), and growth was very slow, on the order of 4 - 5 mm per year.

Larvae in the largest size category did not show any trend of increasing size over successive sampling dates in either 1990 ( p = 0.909) or 1991 ( p = 0.656), but were gener- ally larger in 1991 than in 1990 (ANOVA, F, , = 22.05, p < 0.001).

Discussion Larvae of C. nigripes and Chrysops probably zinzalus in Iron Arm Fen appear to grow very slowly, since newly hatched

tabanid larvae measure 1-2 mm in length (Philip 193 1) and larvae of C. nigripes must reach at least 14 - 16 mm in order to pupate (Teskey 1969). Our finding that larvae of C. nigripes and Chrysops probably zinzalus increase in length at a rate of 14- 19% annually suggests that Chrysops larvae in Iron Arm Fen require at least 7 - 8 years to complete development.

Many temperate-zone tabanid species can complete their development in 1 year (Philip 193 1 ; Logothetis and Schwardt 1948; Jones 1953; Schomberg and Howell 1955; Ellis and Hays 1973; Terterian 1985), although in some species the majority of individuals have a 1-year life cycle, but certain slow-growing individuals require an additional year to com- plete their development (Stone 1930; Logothetis and Schwardt 1948; Tashiro and Schwardt 1953; Magnarelli and Anderson 1978; Terterian 1985). Other large tabanid species always require 2 or more years to complete development under field conditions (Lewis and Jones 1955; Roberts and Dicke 1964; Freeman and Hansens 1972; Meany et al. 1976).

At subarctic latitudes, wetland substrates may be frozen for 8 months of the year or more, meaning that tabanid larvae must spend long periods in winter dormancy. Even during the frost-free period, active larvae have to contend with an environment that is generally cooler than a similar habitat in the south. The long life cycle of Chrysops spp. at Schefferville is doubtless a consequence of the abbreviated growth season there and a relatively cold larval habitat during the growing season. The upper 5 - 10 cm of peatland substrate, where tabanid larvae are found (Miller 1951), thaws for 5 months at most, from mid-May until late September. The tempera- ture of the substrate is higher than 10°C for only about 3 months (Fig. 1). In New York State, where Logothetis and Schwardt (1948) found that Chrysops vittatus Wiedemann had a 1-year life cycle, the ground is unfrozen for the 8 months between early April and late November, and temperatures during this period are, on average, considerably higher than 10°C. In Florida, where C. vittatus has two generations per year (Jones 1953), the ground remains relatively warm and larval development continues year-round.

The trend of gradually increasing larval length over suc- cessive sampling intervals, which was apparent in the 1990 length-frequency distributions of midsized C. nigripes larvae (Fig. 3A) and Chrysops probably zinzalus (Fig. 4A), appears to be continued in the 1991 length-frequency distributions. For Chrysops probably zinzalus, the trend over successive sampling periods in 1990 was toward a progressively increas- ing frequency of larger larvae in the 7- to 10-mm size category, a trend that continued in 1991 for larvae in the 8- to 12-mm size category. If larval recruitment is constant between years, one would expect larval length-frequency distributions to show much more overlap, since seven or eight cohorts would be simultaneously co-occurring within the fen. The fact that only three size categories were present suggests that in some years there is little or no recruitment of larvae, whereas in others many larvae enter the population.

In 1990, adult C. nigripes and Chrysops probably zinzalus collected at Iron Arm Fen numbered 65 and 242, respectively, while the same catch effort yielded 21 and 237 adults, respec- tively, in 1991 (McElligott 1992). In the summer of 1992, we collected no adult Chrysops spp. during the tabanid flight season. Flight activity of subarctic tabanids is severely cur- tailed or prevented by temperatures below 10°C (McElligott

Can

. J. Z

ool.

Dow

nloa

ded

from

ww

w.n

rcre

sear

chpr

ess.

com

by

UN

IV O

F B

IRM

ING

HA

M o

n 11

/09/

14Fo

r pe

rson

al u

se o

nly.

McElligott and Lewis: II 1373

Fig. 3. Total body length (A) and head capsule length (B) frequency distributions for larval Chlysops nigripes Zetterstedt for six successive 2-week periods in 1990 and 1991, in Iron Arm Fen, Labrador.

Sites 1-4

Sites

and Galloway 199 1 ; McElligott 1992), and temperatures during July and August of 1992 rarely surpassed this value. A large number of fully grown larvae were collected at the end of the summer of 1991 (Figs. 3A, 4A), that should have emerged as adults in 1992. During the summer of 1992, mating and host-seeking flights by these adults would have been almost completely prevented, few eggs would have been laid, and therefore recruitment of larvae into the popu- lation would have been minimal.

Unpredictable cold periods could be the main factor affecting recruitment of tabanids at northern latitudes. Fully grown larvae that successfully pupate may, upon emergence as adults, be immobilized by low temperatures. If larval cohorts developed completely synchronously, a given cohort's

reproductive output could be entirely lost because of bad weather during the flight season. Our data show, however, that larvae in a number of size classes are present within a given cohort. Since these larvae grow asynchronously, it is more likely that all larvae do not pupate during the same summer. Owing to the relatively short (3 -4 weeks) Chrysops spp. flight season in the Schefferville area (McElligott 1992), Chrysops probably zinzalus or C. nigripes larvae must pupate within a prescribed 2- to 5-week period in the summer. During what should be their final summer, if larvae have not reached a length of 14 - 16 mm during the period when pupa- tion is possible, they do not pupate at all and continue to grow until they reach their maximum possible individual length of approximately 18- 19 mm. During the following

Can

. J. Z

ool.

Dow

nloa

ded

from

ww

w.n

rcre

sear

chpr

ess.

com

by

UN

IV O

F B

IRM

ING

HA

M o

n 11

/09/

14Fo

r pe

rson

al u

se o

nly.

1374 Can. J. Zool. Vol. 74, 1996

Fig. 4. Total body length (A) and head capsule length (B) frequency distributions for larval Chrysops probably zinzalus Philip for six successive 2-week periods in 1990 and 1991, in Iron Arm Fen, Labrador.

1990 Sites 1-4

(A) 0 Sites 5-8

summer, further growth should occur if larvae have not reached their maximum size, but they presumably pupate as soon as possible.

"Cohort-splitting" life cycles, in which a given cohort emerges over two or three seasons, are typical of a number of insect groups that live in habitats where the growing season is very short, and short periods of growth are separated by long periods of dormancy (Danks 1992). Chironomus spp. (Diptera: Chironomidae) in arctic pools may spend up to 7 years in the larval stage (Butler 1982), and add an additional year to their life cycle if the larvae reach full size too late to emerge in a given summer (Danks and Oliver 1972). A similar pattern of variable life cycle length has been observed in Tipula sacra Alexander (Diptera: Tipulidae) in temperate-zone beaver ponds (Pritchard 1980), in arctic Lepidoptera (Downes 1965), and in subarctic carabid beetles (Kaufmann 1971).

Since larval populations in annual cohorts vary among

peatlands in a given area (McElligott 1992), even if adult emergence from a peatland is low in a given year, many females will likely be active because of emergences from neighbouring peatlands. This ensures that there is always a tabanid population present and ready to take wing when conditions are favourable for adult flight activity.

Acknowledgements

The authors are indebted to Dr. F.G. Whoriskey of the Department of Natural Resource Sciences, McGill University, and two anonymous reviewers for their valuable criticisms of an earlier draft of the manuscript. We also thank summer field assistants A. Chabot and K. Crabb. Funding for this project was initially provided by a Natural Sciences and Engineering Research Council of Canada operating grant to D. J.L. Further financial support was provided by the McGill University

Can

. J. Z

ool.

Dow

nloa

ded

from

ww

w.n

rcre

sear

chpr

ess.

com

by

UN

IV O

F B

IRM

ING

HA

M o

n 11

/09/

14Fo

r pe

rson

al u

se o

nly.

McElligott and Lewis: II

Faculty of Graduate Studies and Research, and the Depart- ment of Entomology through Margaret Duporte Fellowships to P.McE. Logistic expenses for fieldwork were, for the most part, covered by Northern Scientific Training Grants from the Department of Indian and Northern Affairs through the Centre for Northern Studies and Research, McGill University.

References

Butler, M.G. 1982. A 7-year life cycle for two Chironomus species in arctic Alaskan tundra ponds (Diptera: Chironomidae). Can. J. Zool. 60: 58-70.

Danks, H.V. 1992. Long life cycles in insects. Can. Entomol. 124: 167- 187.

Danks, H.V., and Oliver, D.R. 1972. Seasonal emergence of some high arctic Chironomidae (Diptera). Can. Entomol. 104: 661 -686.

Downes, J.A. 1965. Adaptations of insects in the arctic. Annu. Rev. Entomol. 10: 257 -274.

Ellis, H.C., and Hays, K.L. 1973. Population densities of tabanid larvae in two farm pond habitats in east central Oklahoma. Fla. Entomol. 56: 11-14.

Freeman, J.V., and Hansens, E.J. 1972. Collecting larvae of the srlt marsh greenhead Tabanus nigrovittatus and related species in New Jersey: comparison of methods. Environ. Entomol. 1: 653 -658.

Jones, C.M. 1953. Biology of Tabanidae in Florida. J. Econ. Entomol. 46: 1 108 - 1 109.

Kaufmann, T. 1971. Hibernation in the arctic beetle, Pterostichus brevicornis, in Alaska. J. Kans. Entomol. Soc. 44: 8 1 -92.

Lauzon, M., and Harper, P.P. 1993. The life cycle of the aquatic snipe fly Atherix lantha Webb (Diptera: Athericidae) in Quebec. Can. J. Zool. 71: 1530-1533.

Lewis, L.F., and Jones, C.M. 1955. The biology of tabanids in the Mississippi - Yazoo Delta. J. Econ. Entomol. 48: 609 - 6 10.

Logothetis, C., and Schwardt, H.H. 1948. Biological studies on the horse flies of New York. J. Econ. Entomol. 41: 335 -336.

Magnarelli, L.A., and Anderson, J.F. 1978. Distribution and development of immature salt marsh Tabanidae (Diptera). J. Med. Entomol. 14: 573 - 578.

Maire, A. 1984. Les taons (Diptera: Tabanidae) d'une tourbikre B palses situCe B la limit des forCts (Nouveau-QuCbec). Can. Entomol. 116: 1679 - 1682.

Martin, J.E. 1977. Collecting, preparing, and preserving insects, mites, and spiders. The insects and arachnids of Canada. Part 1. Ministry of Supply and Services, Canada, Ottawa.

McElligott, P.E. 1992. Aspects of the biology of horse flies and deer flies (Diptera: Tabanidae) in subarctic Labrador: larval distribution and development, biology of host-seeking females, and effect of climatic factors on daily activity. Ph.D. thesis, McGill University (Macdonald Campus), Ste Anne de Bellevue, Que.

McElligott, P.E., and Galloway, T.D. 199 1. Daily activity of horse flies (Diptera: Tabanidae) in northern and southern Manitoba. Can. Entomol. 123: 361 -370.

McElligott, P.E., and Lewis, D .J. 1994. Relative efficiencies of wet and dry extraction techniques for sampling aquatic macro- invertebrates in a subarctic peatland. Mem. Entomol. Soc. Can. 169: 285 -289.

Meany, R.A., Valeila, I., and Teal, J.M. 1976. Growth, abundance, and distribution of larval tabanids in experimentally fertilized plots on a Massachusetts salt marsh. J. Appl. Ecol. 13: 323 -333.

Miller, L.A. 195 1. Observations on the bionomics of some northern species of Tabanidae (Diptera). Can. J. Zool. 29: 240 -263.

Philip, C.B. 1931. The Tabanidae (Diptera) of Minnesota, with special reference to their biology and taxonomy. Univ. Minn. Agric. Exp. Sta. Tech. Bull. No. 80.

Pritchard, G. 1980. Life budgets for a population of Tipula sacra (Diptera: Tipulidae) . Ecol . Entomol . 5: 165 - 173.

Pritchard, G., and Hall, H.A. 197 1. An introduction to the biology of craneflies in a series of abandoned beaver ponds, with an account of the life cycle of Tipula sacra Alexander (Diptera: Tipulidae). Can. J. Zool. 49: 467 -482.

Roberts, R.H., and Dicke, R.J. 1964. The biology and taxonomy of some immature Nearctic Tabanidae (Diptera). Ann. Entomol. Soc. Am. 57: 31-40.

SAS Institute Inc. 1985. SAS user's guide: statistics. SAS Institute Inc., Cary, N.C.

Schomberg, O., and Howell, D.E. 1955. Biological notes on Tabanus abactor Phil. and T. equalis Hine. J. Econ. Entomol. 48: 618-619.

Stone, A. 1930. The bionomics of some Tabanidae (Diptera). Ann. Entomol. Soc. Am. 23: 261 -304.

Tashiro, H., and Schwardt, H.H. 1953. Biological studies of horse flies in New York. J. Econ. Entomol. 46: 813 -822.

Terterian, A.E. 1985. Bioecological peculiarities of immature stages of horse flies in the U.S.S.R. (Diptera: Tabanidae). Myia, 3: 485-514.

Teskey, H.J. 1969. Larvae and pupae of some eastern North American Tabanidae (Diptera). Mem. Entomol. Soc. Can. No. 63.

Teskey, H.J. 1983. A revision of the eastern North American species of Atylotus (Diptera: Tabanidae) with keys to the adult and immature stages. Proc. Entomol. Soc. Ont. 114: 21 -43.

Can

. J. Z

ool.

Dow

nloa

ded

from

ww

w.n

rcre

sear

chpr

ess.

com

by

UN

IV O

F B

IRM

ING

HA

M o

n 11

/09/

14Fo

r pe

rson

al u

se o

nly.