Polar Biol (1991) ll: 379-383

~s' Springer-Verlag 1991

Short note

A further contribution on the biology of the Antarctic flea, Glaciopsyllus antarcticus (Siphonaptera: Ceratophyllidae) M.D. Whitehead*, H.R. Burton, P.J. Bell**, J.P.Y. Arnould*** and D.E. Rounsevell****

Biology Section, Australian Antarctic Division, Channel Highway, Kingston, Tasmania 7050, Australia

Received 23 June 1989; accepted 19 May 1991

Summary. Experiments showed that adult Antarctic Fleas Glaciopsyllus antarcticus preferred dark over light condi- tions, dry over wet conditions, and fine substrate over coarse substrate. Examination of seabird chicks and col- lections of nest material indicated that the Southern Fulmar Fulmarus ,qlacialoides, is the major host species of the Antarctic Flea, while Snow Petrels Pagodroma nivea, Cape Petrels Daption capense, Antarctic Petrels Thalas- soica antarctica, and Wilson's Storm-Petrels Oceanites oceanicus are minor hosts. This is the first report of Antarctic Fleas occuring on either Antarctic Petrels or Wilson's Storm-Petrels. No fleas were found associated with Southern Giant Petrels Macronectes 9iganteus, Antarctic Skuas Catharacta maccormicki, or Adelie Penguins Pygoscelis adeliae. No live fleas were found in Southern Fulmar nest material during their period of dispersal over the winter months, supporting the hypoth- esis that Antarctic Fleas survive the winter period by remaining on their seabird host.

Introduction

The Antarctic Flea, Glaciopsyllus antarcticus (Smit and Dunnet 1962) is the only species of flea recorded from the Antarctic continent, and the only ceratophyllid found on seabirds inhabiting Antarctic oceans (Smit and Dunnet 1962). To date, it is Earth's most southern-known holo- metabolous insect.

Adult fleas have been recorded in nests of Southern Fulmars Fulmarus 9lacialoides, Snow Petrels Pagodroma

Present addresses: * Department of Ecology and Evolutignary Biology, Monash Uni- versity, Clayton, Victoria 3168, Australia ** Conservation Commission of the Northern Territory, PO Box 496, Palmerston, Northern Territory 0831, Australia *** British Antarctic Survey, High Cross, Madingley Road, Cam- bridge CB30ET, UK **** Tasmanian Department of Lands, Parks and Wildlife, GPO Box 44A, Hobart, Tasmania 7001, Australia

Offprint requests to." M.D. Whitehead

nivea, and Cape Petrels Daption capense, near Casey (66c'17'S, 110~ (Murray et al. 1967), Davis (68~35'S, 77c'58'E) (Rounsevell and Home 1986) and Mawson (67~ 62~ (Murray 1967). Other locally nesting seabird species have not been searched, and factors deter- mining host suitability have not been established.

Until the recent work by Bell et al. (1988), little was known of the life-cycle of G. antarcticus. They found that the life-cycle of the flea was closely synchronised with the breeding cycle of the host. The flea eggs were laid in the nest during the host incubation period and the last of the adults emerged from cocoons just before the fledging of the Southern Fulmar chicks. Throughout its period of repro- duction, the Antarctic Flea was host bound, and not a typical 'nest-flea' (Bell et al. 1988). Fleas associated with migratory birds generally remain dormant in the nests as larvae, pupae or adults (Dunnet 1970) while the hosts are away. However, Bell et al. (1988) suggested that this was not the case with G. antarcticus. The majority of nests examined after chick fledging were free of fleas despite having contained chicks with high flea loads. They hypo- thesized that fleas remained on the host birds over winter, but were never able to search in nest material at a time when the seabird hosts had all departed from the colony during the period between breeding seasons. At the con- clusion of their study, some live adult fleas were still present in the Southern Fulmar colony.

The present contribution reviews all records of known G. antarcticus host species and reports observations from searches of nest material of seabirds not previously con- sidered; examines habitat preferences of adult fleas in terms of light regime and substrate size and moisture level; and explores the hypothesis that adult G. antarcticus over- winter on the host species (Bell et al. 1988).

Methods

Habitat preferences

Choice experiments were conducted to determine the preferences of adult fleas for either moist or dry substrates, illuminated or dark

380

conditions and differing substrate sizes. The experiments were carried out in the laboratory in 9.5 cm diameter glass petri dishes at 15C-+ 2~ Fleas were maintained in dark conditions at 6~ for 24 h before each experiment. At the beginning of each experiment eight fleas were distributed in the petri dishes at random. Different fleas were used for each experiment.

The first experiment tested for light regime preference. One half of a petri dish and its lid were painted black to exclude light and the fleas were introduced on a dry filter paper. The dish was illuminated from above and counts of fleas in the unpainted side of the dish made over four 20 rain intervals. The experiment was repeated twice.

The second experiment tested for moisture preference. Fleas were placed on a 9 cm filter paper moistened on one half of its area. After 20 min the fleas on the moist side were counted and the dish was rotated through 180 ~ on the vertical axis. Three further counts were made at 20 rain intervals, the dish being rotated each time. This experiment was repeated twice.

The third experiment tested for substrate size preference. Coarse sand was placed in one half of three petri dishes with either fine, medium, or very coarse sand in the other halves. This sand was sieved from Snow Petrel nest material. Counts were made of the fleas remaining on each substrate type over four 20 rain intervals as in the previous experiments. This experiment was repeated once.

Host species

During the period between 1962 and 1982, various searches were made of the nest material of different seabird species in order to establish which birds were hosts to the Antarctic Flea. These searches were made in December 1969, January 1973, January 1974 and January 1982 in the Vestfold Hills region (68~ 78~ and at Ardery Island near Casey (68~ 110~ between November 1986 and March 1987. In some cases they consisted of in situ examination of the nest and in others a sample of nest material was collected and returned to the laboratory for sorting. In cases where material was examined in the field, either presence/absence or an approximation of the number of adult and larval fleas was made. Accurate counts were made of material sorted in the laboratory. During a bird banding program on Ardery Island, chicks of the Southern Fulmar, Antarctic Petrel Thalassocia antarctica, Cape Petrel, Snow Petrel and Wilson's Storm-Petrel Oceanites oceanicus, were examined for infestation by the Antarctic Flea.

The size distribution of nest material sediment was determined for 6 Cape Petrel and 6 Snow Petrel nests by sieving the material through a graded series of sieves according to the Wentworth particle size classification (Holme and Mclntyre 1971).

Over-wintering strategy

Twenty-five Southern Fulmar nests were collected from the Rauer Islands (68~ 77~ in south-east Prydz Bay on 15 September, 7 November and 21 December 1987. On 15 September, material was collected from 10 nests known to have been heavily infested with fleas the previous summer. No birds had been present in the colony since chick fledging in March of the previous season. On 7 November

material was collected from 5 nests occupied by courting birds, and further material was collected from 10 nests occupied by incubating birds on 21 December.

The nest material consisted of rocks, gravel, sand and feathers. It was collected to a depth of 5 10 cm or to bedrock. In September, the nest sites were covered by up to 30cm of snow and the nests themselves often consisted of a frozen accretion of water, sediment and feathers. In November the nest material was still frozen, but not covered by snow. The material was stored in open plastic bags at ambient temperatures until examination in the laboratory using a dissecting microscope.

Results

Habitat preferences

Data from the replicates and time intervals of each experi- ment were pooled, as chi-squared analyses showed no significant differences between them. Chi-squared analyses of pooled data for each experiment indicated that: (i) a significant preference existed for dark over i l luminated condi t ions (Z2=12.5, d f = l , P<0 .005) (Table 1). (ii) a significant preference existed for dry condi t ions over wet condit ions (~2 = 32.5, df = 1, P < 0.005) (Table l) and, (iii) a significant preference existed for fine sand over coarse sand (ZZ= 8.5, d f = 1, P <0.005), but not for coarse over very coarse, or coarse over medium (Table 2).

Host species

We have summarised the results of our searches for host species, and those of previous authors in Table 3. Of the eight seabird species examined, we recorded the Antarctic Flea occurring on five of these, including the Antarctic Petrel and Wilson's Storm Petrel, from which it has not been documented previously. The Southern Fu lmar ap- pears to be the major host, fleas occurring on the great majori ty of chicks, and in most nests examined dur ing the chick-rearing period. Antarctic Petrel, Cape Petrel, Snow Petrel and Wilson's Storm-Petrel were infested less con- sistently, and though there were instances when infes- tat ions seemed relatively high when these species were in the proximity of nesting Southern Fulmars , the relative abundance of fleas on isolated popula t ions of Snow Petrel at Davis indicates that this does not exclusively apply (Table 3).

The Snow Petrel nests contained five times as much fine sand as the Cape Petrel nests (Table 4), probably because of their greater protect ion from wind in the

Table 1. Counts of fleas given choice of light or dark conditions and wet or dry conditions

Time elapsed (min) Number of fleas on different treatment (~-+SD)

Light Dark Wet Dry

20 1.67_ 1.53 6.33_+ 1.53 0.33___0.58 7.67-+0.58 40 1.67-+0.58 6 .33-+0 .58 0 .67-+1 .15 7.33_+1.15 60 2.00 • 1.00 6.00 _+ 1.00 1.00 • 1.00 7.00 • 1.00 80 2.67_+2.08 5.33• 0.67_+0.58 7.33_+0.58

crevices they occupy. Though we did not measure the nest sediment size frequency dis t r ibut ion of Southern Fu lmar or Antarct ic Petrel nests, we did observe that Antarct ic Petrel nests were often on open rocky ledges and not on sand, though many of the Southern F u l m a r nests were. A visual compar ison of Southern F u l m a r and Antarctic Petrel nests on Hop Island in the Rauer group indicated that Antarct ic Petrel nests have generally less material, with a relatively greater p ropor t ion of pebbles than sand and detritus (G.W. Johnstone, personal communicat ion) .

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Over-winterin9 strategy

No live fleas of any stage in the life-cycle were found in the Southern Fu lmar nest material collected in September or November. Varying numbers of dead specimens were found in this material. In the December samples, live adult fleas, as well as dead specimens, were found (Table 5).

Dur ing the December sampling, five incubat ing South- ern Fulmars were examined. Blood faeces were clearly visible on the breast and a round the brood patch on three

Table 2. Counts of fleas given choice of different substrate sizes. Data from both trials of the experiment are given. Particle sizes as indicated in Table 4

Time elapsed (rain)

Number of fleas on different substrates (2_+ SD)

Very coarse vs. Coarse Coarse vs. Medium Coarse vs. Fine

20 4 4 4 4 2 6 5 3 5 3 2 6

40 3 5 3 5 1 7 5 3 4 4 1 7

60 4 4 2 6 3 5 6 2 3 5 1 7

80 3 5 4 4 4 4 4 4 3 5 3 5

Table 3. Summary of searches for the Antarctic Flea in the nests, and on the bodies of chicks of various seabird species. NR = not recorded

Seabird Location Date No. nests or Results/comments Source species lat. S, long. E chicks examined

Southern Fulmar

Antarctic Petrel

Snow Petrel

Ardery Is. NR nests adult fleas Murray et al. 66 22, 110 27 present (1967)

Nov 86- 75 nests all stages isolated Bell et al. (1988) Mar 87 found population " 105 chicks 75 infested (larvae, pupae~ Bell et al. (1988)

adults); 30 not infested Rauer group 9.1.73 1 nest >20 adult fleas This study 68 51, 77 50

4.1.82 nests adult fleas in virtually This study all nests

" NR nests nests infested Rounsevell and Horne (1986)

Rauer group 4.1.82 34 nests 14 with This study fleas; 20 with no fleas

Ardery Is. Nov 86- 25 nests 9 with fleas near Southern This study Mar 87 (all stages), 16 Fulmars

with no fleas . . . . 16 chicks 5 infested (larvae, pupae, This study

adults); 11 not infested

Anchorage Is. 28.12.61 nests 4 adult fleas 68 34, 77 56 1 pupae Gardner Is. 26.12.69 1 nest adult fleas 68 35,77 52 present

Jan 1974 nests fleas present

Brown (1966)

This study

Rounsevell and Horne (1986)

(continued on next page)

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Table 3 (continued)

Seabird Location Date No. nests or Results/comments Source species lat. S, long. E chicks examined

Cape Petrel

Wilson's Storm Petrel

Southern Giant Petrel

Antarctic Skua

Bluff Is. Jan 1974 nests fleas present 68 33, 77 54 Magnetic Is. NR nests fleas present 68 33, 77 54 Clear Lake 31.1.74 6 nests 83 adult fleas; isolated 68 39, 78 00 325 larvae population Stalker Hill Jan 1974 nests fleas present 6831, 7827 Tryne Fjord Jan 1974 nests fleas present 68 28, 78 22 Masson Range NR nests numerous adult 67 45, 62 55 fleas and larvae Ardery Is. Nov 86- 20 nests 2 nests with fleas; isolated

Mar 87 18 nests with population no fleas

. . . . 20 chicks 3 infested; 17 not infested

Gardner Is. 26.12.69 5 nests 3 nests with near Snow adult fleas; 2 with Petrel nests no fleas

Bluff Is. Jan 1974 12 nests Nil Jan 1974 6 nests 2 adults near Snow

3 larvae Petrel nests Magnetic Is. 9.1.82 9 nests Nil Vestfold Hills NR nests present islands Ardery Is. Nov 86- 23 nests 8 nests with near Southern

Mar 87 fleas (all stages); Fulmars 15 nests with none

. . . . 8 chicks 6 infested (larvae, pupae adults); 2 not infested

Vestfold Hills Jan 1974 4 nests Nil 68 33, 78 15 Ardery Is. Nov 86- 6 nests 2 with fleas near Southern

Mar 87 (larvae & adults), Fulmars 4 with no fleas

. . . . 6 chicks 5 infested (larvae and adults); 1 not infested

Hawker Is. Jan 1974 6 nests Nil 6838, 7751

Vestfold Hills Jan 1974 4 nests Nil Ardery Is. Nov 86- 2 nests Nil

Mar 87 Adelie Penguin Vestfold Hills Jan 1974 24 nests Nil

Rounsevell and Horne (1986) Murray (1967)

This study

Rounsevell and Home (1986) Rounsevell and Horne (1986) Murray (1967)

This study

This study

This study

This study This study

This study Rounsevell and Horne (1986) This study

This study

This study

This study

This study

This study

This study This study

This study

Table 4. Size distribution of nest material from Cape Petrel and Snow Petrel nest sites

Particle size (mm) Percentage composition (dry wt)

(Wentworth scale) Cape Petrel (n = 6) Snow Petrel (n = 6)

<0.25 (fine sand) 1.3 >0.25 <0.50 (medium sand) 7.2 >0.50< 1.00 (coarse sand) 15.5 > 1.00 < 2.00 (very coarse sand) 13.5 > 2.00 (gravel and rock) 62.5

6.5 12,5 12.0 8.5

60,5

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Table 5. Flea specimens found in Southern Fulmar nests between September and December 1987

Sample Date

15 September 7 November 21 December

1 1 dead adult 2 1 dead adult

1 adult exuvium 3 4 dead adults

1 adult exuvium 2 larval exuvia

4 7 adult exuvia 5 2 adult exuvia

1 dead larva 6 7 dead adults 7 4 dead adults 8 9 10

1 dead adult 1 live adult 1 dead adult 1 live adult

2 dead adults 1 live adult

4 live adults

of the birds, and one live adult flea was found on the breast of one of the birds.

Discussion

The habitat characteristics preferred by the Antarctic Flea would be beneficial in minimising the chance of desicca- tion in the dry Antarctic summer, without risk of drowning in areas of melt runoff or water accumulation. Observa- tions of the substrate composition of the nests of the four host species suggest that the nests of Southern Fulmars and Snow Petrels are more suitable as flea habitats than the nests of either Antarctic Petrels or Cape Petrels. The work by Bell et al. (1988) has suggested that the role of the host nest in the life cycle of G. antarcticus may not be as important as suggested by earlier workers (Murray et al. 1967; Rounsevell and Home 1986). As flea larvae occur on the body of host chicks (Bell et al. 1988), the host nest may only be involved as a site in which to lay eggs and as a temporary refuge for some adult and larval individuals. Therefore, factors other than the nature of the host nest are probably more important in determining the suitability of seabirds as host species. Further survey is necessary, taking into account location of each nest relative to those of the same and other host species, shelter, social behavi- our of the seabird, water drainage and so on, so these may be elucidated.

No living stage of the Antarctic Flea remained in the host nest material during the winter months, when the Southern Fulmars remain distant from their breeding colonies, unlike other fleas associated with migratory birds (see Schelhaas and Larson 1989). The only plausible explanation for this is that they remain on the host during the winter period. Remaining on the bodies of their seabird host seems to be Glaciopsyllus' choice of hibernacula, and strategy of freeze-avoidance during the extreme temper- atures of the Antarctic winter. An examination of host

species obtained at sea during the winter and early spring may conclusively establish this strategy of survival. Dead fleas found in the nests over the winter months probably starved subsequent to the departure of their hosts in the previous summer, as Bell et al. (1988) found some live adult fleas remaining in the nests shortly after the fledging of chicks.

The low numbers of live adult fleas present in the nests of incubating birds in late December also agrees with the hypothesis of Bell et al. (1988) that many adult fleas remain on the host bird.

The frozen nest material during the winter months is unlikely to be suitable for over-wintering survival of the flea. When the ice-bound nest material thaws, it becomes very wet; representing a further hazard to the flea. Spring flooding has been suggested as a threat to the survival of aggregations of Antarctic Tick Ixodes uriae also (Lee and Baust 1987).

The paucity of knowledge regarding overwintering physiology of ectoparasitic insects (Schelhaas and Larson 1989), particularly in Antarctica (Lee and Baust 1987), and Glaciopsyllus' unique biogeographic position within the insect world, indicate the importance of increased scientific attention to this species.

Acknowledgements. We are grateful to R. McLean and the late G.W. Johnstone for making the observations in 1969 and 1982 respec- tively. P. Osborne and P. Butler provided valuable assistance in obtaining the nest material. E.J. Woehler kindly commented on an earlier draft, and the suggestions of three anonymous referees improved the manuscript.

References

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Rounsevell DE, Horne PA (1986) Terrestrial, parasitic and intro- duced invertebrates of the Vestfold Hills. In: Pickard J (ed) Antarctic oasis, terrestrial environments and history of the Vestfold Hills. Academic Press, New York London, pp 309 331

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