A comparative approach to the entomological diversity of polar regions

Acta Oecologica

19 (3) (1998)

303-308

/ 0 Elsevier,

Paris

A comparative approach to the entomological diversity of polar regions Philippe

Vernon

’ *, Guy Vannier

2, Paul Trehen

’

. ’ UMR 6553, CNRk, ’ URA 1183 CNRS,

uniumitd Laboratoim

de Renna 1, Stution biologique, 35380 Paimpont, France. d’kdogie g&n&ale, Mus&m national d’histoire naturelk, 4 avmue du Petit ChBteau, 91800 Brunoy, France * Corr+mding author (e-mail: philiple.uernon~uni?l-rmnps I.,& Received

April

1, 1997;

accepted

January

13, 1998

Abstract -The Arctic and Antarctic are both cold deserts but show contrasting geographic and climatic features. Marked differences are noticeable in the richness of insect communities at these high latitudes. In the north, a continuous terrestrial gradient links sub-Arctic and Arctic regions, while in the south, the Southern Ocean is an efficient barrier between the sub-Antarctic and the Antarctic. In spite of stressful environmental conditions, insects are present but species richness is poor. Functional diversity is subordinate to these constrained features. However, ecological and physiological adaptations are varied and generally show no taxonomic pattern. On sub-Antarctic islands, the recent increase in human activities has precipitated a dramatic increase in entomological diversity. In the Arctic, the spectacular underrepresentation of the Exopterygota cannot be explained only by biogeographic criteria. An ecophysiological interpretation is suggested and leads to an evolutionary hypothesis of entomological biodiversity in polar regions. 0 Elsevier, Paris

Arctic

I Antarctic

I biodiversity

I biogeography

I insects

1. INTRODUCTION The study of geographic variation in species diversity is of paramount importance in a changing world [26, 411. There is considerable information on spatial and temporal patterns found in large scale diversity [ 11, 121 with many studies paying specific attention to comparisons of temperate and tropical regions [24.. 591. Investigations of latitudinal gradients across these regions are currently attracting considerable attention. However, comparisons between regions of equal latitude in the northern and southern hemispheres are less common [4, 541. Nonetheless, this kind of approach merits further attention, especially where diversity may be expected to be similarly poor, communities similarly structured, or species to have similar physiological adaptations [78]. Bipolar comparisons may be particularly informative because the areas are amenable to sampling and because their faunas are comparatively well-known. However, comparisons of Arctic and Antarctic terrestrial systems have decreased since the early studies of bipolar distributions and the IBP’s (International Biological Programme) comparisons of northern and southern tundras [40, 57, 601. In this paper, the usefulness of bipolar studies is illustrated by discussing a number of entomological examples. Collembola are not considered here as

belonging to the class Insecta. Particular attention is given to links between entomological diversity and functional diversity in polar ecosystems given that insects are an important group in both the Antarctic and Arctic by virtue of their species richness, functional roles and diversity of adaptations [77]. Reviews of insect biodiversity in the Arctic and Antarctic can be found in Block [5], Chemov [14], Danks [28, 301 and Somme [66]. 2. BIOGEOGRAPHICAL DIFFERENCES BETWEEN THE ANTARCTIC AND THE ARCTIC The symmetrical polar positions of the Arctic and Antarctic belie rather different geographical situations: the Arctic is an extension of a continental mass which is fragmented into several archipelagoes in its northern part; whereas, the Antarctic is a continental mass which is isolated from the other continents by a wide oceanic belt (c. from 66” S to 40” S) [61]. The subAntarctic islands, Southern New Zealand and Tierra de1 Fuego are the only terrestrial areas that penetrate this oceanic zone. This geographic imbalance is partially responsible for the climatic differences between these regions [68]. At the same latitude, annual mean temperatures are generally higher in the Arctic

304 (warmer summers) than in the Antarctic. In the subArctic, the polar climate rapidly improves while in the sub-Antarctic, the climate is cold oceanic (annual mean temperatures only slightly higher than 0 “C and mean annual precipitation greater than 1 000 mm). Arctic and Antarctic climatic features are discussed in detail by Dar&s [28] and Walton [80]. A convenient classification scheme for climates of polar regions is given by Young [81]. At identical latitudes, landscapes also differ considerably between north and south. For example, at the polar circles (66”), boreal tundra is found in the Arctic, whereas a polar desert, dominated by mosses and lichens, is characteristic of the Antarctic. As a consequence, the free-living entomofauna of the Antarctic is extremely poor: only two species of Diptera (Chironomidae) are found on the Antarctic Peninsula [5]. The limit of distribution of these species is 62” 37’ S for the winged midge Parochlus steinenii [37] and 68” 17’ S for the wingless midge Belgica antarctica [75]. On the sub-Antarctic islands, free-living insect species richness is not particularly high. Coleoptera and Diptera predominate (e.g. 63 % of the fauna at Marion and Prince Edward Islands and 80 % at Heard and MacDonald Islands). Total species richness varies from 10 species at Heard and McDonald Islands (380 km2) to 51 species on the Crozet Islands (500 km2) [18, 39, 421. It is noteworthy that the two largest sub-Antarctic islands, South Georgia (3 800 km2) and Kerguelen (7 000 km2), have an intermediate number of insect species (30 and 31 species respectively). All of the sub-Antarctic islands are extremely isolated (continents > 1 000 km) and consequently it appears that the classic relationship of species number to area and distance does not apply; this is an exception to the predictions of the equilibrium theory of MacArthur and Wilson [50]. In the Arctic, species richness is far higher. For example, 198 species of insects have been recorded at Barrow, Alaska (71” N): 11 orders are present, but a single order, the Diptera, accounts for 66 % (133 species) of the insect fauna [36]. At Bathurst Island (75” N), 61 species from three orders have been recorded with 54 species of Diptera (89 %) [27]. At higher latitudes, such as Isachsen, Ellef Ringnes Island (78” N), 27 species from three orders have been recorded, of which 25 (93 %> are Diptera [49]. The incidence of flightlessness in these insects increases with latitude, probably for ecological reasons (environmental homogeneity) [58]. Currently, the Canadian Arctic Islands are known to contain 462 insect species, of which 307 are Diptera [30]. This value may be compared with the 51 species of Diptera known from the sub-Antarctic islands (Vernon, unpubl. data). As a comparison, in Great

P. Vernon

et al.

Britain some 22 000 insect species (of which 6 000 are Diptera) have been described [45, 721. Interestingly, when micro-arthropods (Collembola and Atari) are compared in a similar way, far fewer differences between the north and south polar regions emerge, e.g. 20 species of Collembola in the Antarctic (60” - 90” S) vs. 41 species in Greenland (60” - 84” N) [65] or 528 species of Atari in the Antarctic and sub-Antarctic vs. 386 species in the North American Arctic [28, 561. Of the Atari, the oribatid mites are widely distributed throughout the polar regions, e.g. 11 species in the maritime Antarctic islands, 9 species in Heard Island, 31 species in South Georgia (sub-Antarctic) and 33 species in the High Arctic [8, 28, 70, 711. In the sub-Antarctic, a rapid and dramatic increase in the number of insect species is currently being observed, with noticeable differences between islands (from one alien species at Heard and MacDonald Islands to 12 alien species at South Georgia). These accidentally introduced species are frequently saprophagous Diptera (Chironomidae, Sciaridae, Sphaeroceridae, Calliphoridae), but also phytophagous Lepidoptera (Plutella xylostella at Marion Island) or predaceous Coleoptera (Trechisibus antarcticus at South Georgia and Ooptems soledadinus at Kerguelen Islands) [15, 20, 38,]. These species are of special interest since their introduction or colonization can be monitored in the sub-Antarctic (island isolation), but it is impossible to do so in the Arctic (contiguity to the continental land masses). In the sub-Antarctic and the Arctic, the role played by decomposers is particularly important as these two biomes are decomposition-based. Hence, the functional diversity of these systems is under the close dependence of the low species diversity of insect communities [5, 301. 3. INSECT ADAPTATIONS TO COLD TEMPERATURES ARE NOT SPECIFIC TO THE POLAR REGIONS Antarctic, sub-Antarctic and Arctic insects are confronted by harsh environmental conditions with which they cope using various behavioural and ecophysiological strategies [48, 511. In this respect, cold-hardiness is a key factor, since insects must survive low temperatures during winter (generally in an inactive state), but also during summer, the only time available for growth and reproduction. Nonetheless, it appears that these adaptations are not fundamentally different from those described in insects in alpine or even temperate zones [68, 691. Some insects are able to survive the formation of ice in their tissues (freezing tolerance) but, generally, ice formation is lethal (freezing intolerance). Freezingsusceptible insects depend on supercooling to survive Acta

Oecoiogica

Entomological

diversity of polar zones

305

temperatures below the freezing point of their body fluids [6, 661. The supercooling point is the lowest temperature at which the undercooling of body fluids ceases and spontaneous freezing occurs. It may be considered as the potential lower limit for survival of a freezing-intolerant species at any given stage [76, 791. In an enlarged classification of insect cold-hardiness, Bale [l] emphasizes that freezing tolerance and intolerance are the endpoints of a continuum. Evolutionary trends which may lead a species to become freezing tolerant or intolerant remain obscure. A classification based only on simple ecological or systematic factors is impossible. It appears that small species (or small sized stages of development such as eggs) are associated with a high proportion of freezing intolerance [68]. Moreover, some species experience the two conditions during their life cycle: e.g. the larvae of Belgica antarctica are freezing tolerant, whereas the adults are freezing intolerant [2, 231. In the Arctic, freezing intolerant insects frequently display very low supercooling points, e.g. -58” C in the cecidomyiid fly Rhabdophaga strobilioides [52]. Freezing tolerance is common and “supposed to be likely in insects from regions where winters are especially cold, such as the Arctic (e.g. Downes [35]), because supercooling is difficult to achieve at very low temperatures and for very long periods” [33]. It seems that the current success of several newly introduced insect species in the sub-Antarctic and in the maritime Antarctic, may partially be explained by the fact that many species have a sufficient level of cold adaptation (i.e. pre-adaptation) [9]. 4. TWO QUESTIONS INTEREST

OF

EVOLUTIONARY

4.1. Why the low level of phytophagy tion-based systems ?

in decomposi-

Both in Arctic and sub-Antarctic terrestrial ecosystems, there are few species of vascular plants and few herbivores. Fellfield communities, where bryophytes and lichens predominate, are present even at low altitudes [ 19, 281. On sub-Antarctic islands, predators are scarce in terrestrial systems, and food webs are principally detritus-based. The majority of the energy and nutrients entering such systems is of marine origin and derived from faecal output of seabirds and pinnipeds [63, 64, 731. Even the endemic, phytophagous fly Culycuptelyx mosekyi (Micropezidae), which lives on the Kerguelen cabbage Pringlea antiscorbutica, shifts its feeding regime towards saprophagy when cabbages disappeared because of introduced rabbits [74]. One consequence of having few herbivores is that plants seem to be devoid of adaptations which may restrict herbivory 1431. Therefore, when introduced, herbivoVol. 19 (3) 1998

rous mammals have severe effects on the vegetation [13, 471. In this context, it is worth noting that on the Crozet Islands, the 12 Diptera species are largely saprophagous, and 15 of the 23 Coleoptera species belong to the phytophagous family Curculionidae [21]. Habitat use by insects on Possession Island is discussed in detail by Davies [34] who found that the fellfield, in spite of its scant vegetation, permitted the existence of a relatively species-rich weevil community. In addition, the ecology and biogeography of the sub-Antarctic weevils have been extensively studied by Chown [16, 18, 191. He recognized two major groupings based on habitat use and diet: i) species which feed on angiosperms, but not exclusively as more or less pronounced switches to cryptogams are observed; ii) species which feed on bryophytes, an uncommon feature for curculionids [ 191. Two hypotheses have been proposed to explain the high incidence of bryophyte herbivory in polar terrestrial vertebrates and invertebrates. The physiological hypothesis proposes that arachidonic acid, a fatty acid abundant in certain bryophytes might provide complementary cryoprotection for cell membranes [55]. Thus, at low temperatures, bryophagy may develop so that animals can benefit from this fatty acid. This assumption is challenged by Crafford and Chown [25] who argued that bryophyte feeding does not seem to be nutritionally more advantageous at low temperatures. The second essentially historical hypothesis considers the possible role of Quaternary climatic events, and particularly the extent of glaciations, on the specific composition of sub-Antarctic vascular vegetation [17]. Current angiosperms are likely to be of post-glacial origin, even if some refugia existed during the past glaciations [62]. So, bryophagy might characterize ‘old’ species while radiation of ‘young’ species may be observed since the recolonization of the sub-Antarctic islands by an angiosperm flora [19]. Bryophagy as an alternative to extinction illustrates the fact that some current trophic functions may be adaptations to previously existing conditions. Identifying such constraints is of value when present patterns are being interpreted [lo]. 4.2. Why so few exopterygote Arctic?

insect species in the

The majority of insect species are endopterygote (distinct larval, pupal and adult stages). If we consider the four main orders of holometabolous insects (endopterygote development), i.e. Coleoptera, Hymenoptera, Lepidoptera and Diptera and the three main orders of hemimetabolous insects (exopterygote development), i.e. Dictyoptera, Orthoptera and Hemiptera, we observe that globally 88 % of the species are holometabolous [53].

P. Vernon

306 Table I. Specific

richness

in four hemimetabolous

insect orders

and four holometabolous

Canada 42” N/83”

Latitude Area (km’) Hemimetabolous

N

and three Arctic

Bathurst

Iceland

9 972 800 (number

orders (Canada

65” N 103 000

locations)

[27,29,32,671. Svalbard

75” N

79” N

16 380

62 420

12

of species)

Orthoptera

133

Dictyoptem

17

Hemiptera

3 079

7x

Coleoptera

6 748

239

0

Lepidoptera

4 692

97

2

5

Diptera

7 OS8

373

54

97

Hymenoptera

6 028

2.56

5

23

27 7.55

050

61

145

Holometabolous

Total number

et al.

(number

of species)

of species Holometabolous

xx.4

9 I .9

(%) Diptera

100

25.4

3.53

8X.5

66.9

(%r) Coleoptera

24.3

22.8

0.0

8.3

94.5

(%)

Table I, which summarizes species richness data from Canada and three Arctic localizations (Iceland, Bathurst Island and Svalbard), shows that, in the Arctic, very few insect species are exopterygote. It also shows the dramatic dominance of Diptera. Only a few families of Diptera (e.g. Chironomidae) are responsible of this pre-eminence. Other orders are underrepresented, principally Coleoptera [28]. The progressive increase in representation of the holometabolous insects at high latitudes may be related to the advantages of the evolutionary decoupling of larval stages (feeding) and adult stages (dispersal and reproduction) [ 31. Holometabolous development might also be associated with a greater nutritional efficiency than in the case of hemimetabolous development. For exopterygote insects, the regular production of a large mass of cuticle is metabolically costly and represents “the great burden of hemimetabolous larval life” [3]. We suggest that in cold regions, the cost of cuticle production may be even higher. Among holometabolous orders, the low representation of Coleoptera in the Arctic (table I), independently of biogeographical history, supports this hypothesis. In beetles, the contribution of the cuticle to adult body mass is unusually high. The role of such a developmental constraint, here identified as a consequence of a comparative ecophysiological approach, should be subject to further scrutiny.

5. CONCLUSION The functional diversity characteristic of Arctic, sub-Antarctic and Antarctic insects is subordinate to the interaction of historical, geographical and climatic factors which have determined in the past, and currently determine, the low species diversity of insect communities. Because of the dominant human influence in temperate and tropical zones, the Arctic and the Antarctic are often considered environments of only marginal interest [36]. Nevertheless, these ecosystems are not simple, but, as emphasized by Danks [30], complexity seems to be more understable here because diversity is not “overwhelming”. So, an extensive approach to colonization processes and survival strategies suffers from insufficient knowledge, even though species richness in these immense regions is poor. This poses a considerable challenge: undertaking such a biogeographical and ecophysiological approach is of importance, given that Arctic and Antarctic insects constitute valuable candidates for assessing the consequences of long-term environmental changes [7, 3 1, 441. Hence, research in these areas should be conducted, particularly in the Arctic and in the sub-Antarctic islands. As a consequence, substantial progress could be made towards linking species and ecosystem perpectives [14, 22, 461.

Entomological

diversity of polar zones

Acknowledgements We thank Lewis Davies for contributions to our thinking for this paper and we are grateful to Steven Chown for critically reading and helping in editing the English version of the manuscript. We are also indebted to the ‘Minis&e de l’education nationale, de l’enseignement sup&ieur et de la recherche (DSPT 5)’ and to the ‘Centre national de la recherche scientifique (Direction des sciences de la vie)’ for financial support (‘Action coordonnee de recherche: reponses adaptatives aux stress environnementaux’).

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