Austral Ecology (2005) 30, 1–13
Does biogeographical history matter? Diversity and distribution of lotic midges (Diptera: Chironomidae) in the Australian Wet Tropics BRENDAN G. MCKIE,1,2,3* RICHARD G. PEARSON1,2 AND PETER S. CRANSTON2,3 1 School of Tropical Biology, James Cook University, Townsville, Queensland, Australia, 2Rainforest Cooperative Research Centre, and 3Entomology Department, University of California, Davis, California, USA
Abstract We examined broad scale patterns of diversity and distribution of lotic Chironomidae (Diptera) within the Wet Tropics bioregion of northern Queensland, Australia. Field surveys across broad latitudinal and altitudinal gradients within the Wet Tropics revealed a fauna of 87 species-level taxa in 49 genera comprising three main elements: a small genuinely tropical fraction, and larger cosmopolitan and Gondwanan components. The latter group originated when Australia, as part of the ancient Gondwana supercontinent, was situated over Antarctic latitudes with a cooler, wetter climate than today. In the Wet Tropics, cool Gondwanan taxa occurred predominantly in upland and shaded lowland sites, but no species appeared narrowly temperature restricted, and there was no faunal zonation with altitude. Most chironomid species occurred at all latitudes within the Wet Tropics, with no evidence for an enduring effect of the historical rainforest contractions on current-day distribution patterns. These findings contrast with those for aquatic faunas elsewhere in the world and for the terrestrial Wet Tropics fauna. We relate this to the generally broad environmental tolerances of Australian chironomids, and comment on why the latitudinal diversity gradient does not apply to the Australian chironomid fauna. Key words: altitude, diversity gradients, faunal zonation, Gondwana, tropical streams.
INTRODUCTION Knowledge of patterns of diversity and distribution of lotic organisms is deficient, especially outside the temperate northern hemisphere and at very large spatial scales (Vinson & Hawkins 1998). Consequently, the applicability of a latitudinal diversity gradient to freshwater ecosystems (Coffman 1989; Flowers 1991) and the generality of the humped relationship between altitude and diversity exhibited by some northern hemisphere systems (Minshall 1985; Casas & VilchezQuero 1993) are both unclear. Previous study of the broad-scale distributional patterns of lotic eastern Australian chironomids, assessed by sampling the cast skins of emerging adults (pupal exuviae) at multiple locations and times within a latitudinal gradient, showed no evidence for a larger regional species pool in the tropics of northern Queensland than in the temperate south-east (Cranston 2000a). Furthermore, species believed restricted to cool south-eastern
*Corresponding author. Present address: Department of Ecology and Environmental Science, Umeå University, SE90187 Umeå, Sweden. E-mail:
[email protected], Fax: + 46 90 7866705. Accepted for publication February 2004.
streams, with biogeographical affinities (sister-taxon relationships) with other Gondwanan landmasses (particularly southern South America and New Zealand) and assumedly from cool-adapted lineages, were found to have anomalous presence in Australia’s tropical north (Cranston 2000a). Here we extend these observations by focusing on patterns of chironomid diversity and distribution within northern Queensland’s Wet Tropics bioregion. In particular, we assess how restricted the cool Gondwanan component is in its distribution within the Wet Tropics. The Wet Tropics bioregion, between the cities of Cooktown and Townsville along the east coast of northern Queensland, Australia (Fig. 1), has high but seasonal rainfall, with summer wet season falls (ca 600 mm/month in the vicinity of Tully Gorge) substantially greater than those of the winter dry season (ca 150 mm/month, Pearson 1994). These conditions favour tropical rainforests, which straddle a spine of mountains that frequently rise to over 1000 m a.s.l. (Nix 1991; Goosem et al. 1999). Beyond the bioregion, the climate is hotter and drier, and rainforest gives way to xeric vegetation types (Switzer 1991). Despite covering just 0.01% of the surface of Australia (1 849 725 ha), the Wet Tropics supports a major proportion of the continent’s terrestrial plant and animal species, including 65% of its fern species, 36%
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of its mammals, 60% of its butterflies and 41% of its freshwater fishes (Pusey & Kennard 1996; Goosem et al. 1999). Regional endemism among the terrestrial fauna is also high, with 25% of the region’s plant and vertebrate species occurring nowhere else (Williams & Pearson 1997; Goosem et al. 1999). Similar data are unavailable for freshwater invertebrates, though diversity of some freshwater insects (notably Trichoptera) appears higher than in comparable areas of south-eastern Australia (Benson & Pearson 1988;
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Lake et al. 1994), in contrast to Cranston’s (2000a) observations for chironomids. The range of rainforests within the Wet Tropics has oscillated with climatic fluctuations during the Quaternary, due to their specific temperature and rainfall requirements (Quilty 1994). Glaciation at higher latitudes was associated with a global reduction in rainfall, and during the last glacial maximum in the Pleistocene (13 000–8000 years ago), most Australian tropical rainforest was displaced by drier sclerophyll
Fig. 1. Locations of surveyed stream sites. Sites are identified further in Table 1. Boxes represent discrete blocks of tropical rainforest.
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forests. Isolated moist refugia did remain, the largest centred on the Thornton and Atherton uplands (Fig. 1, Nix 1991). As the climate ameliorated, rainfall increased and rainforest expanded to its current extent (Hopkins et al. 1996), but modern diversity and distribution patterns of several groups of terrestrial organisms bear the signature of past rainforest contractions. For example, diversity and endemicity of vertebrates are greatest in the large refugial areas, which maintained the largest vertebrate populations during the glacial period (Williams & Pearson 1997; Williams 1997; Winter 1997). Patterns for flightless terrestrial bugs and beetles are more complex, evidently because smaller rainforest refugia maintained significant populations of rainforest arthropods Table 1.
(Yeates et al. 2002; C. A. M. Reid pers. comm., 2000). In contrast, current-day diversity patterns of the Wet Tropics freshwater fish and Trichoptera faunas seem little affected by the Pleistocene contractions, with most species homogeneously distributed throughout the region’s latitudinal range (Pusey & Kennard 1996; Pearson in press). Here we characterize the biogeographical affinities of the regional chironomid fauna, and consider relationships between patterns of diversity and distribution and both historical (the Pleistocene rainforest contractions) and ecological (especially altitude) factors. We examine evidence derived from two species-level surveys of lotic Chironomidae. The first sampled the riffleinhabiting fauna of 32 streams, covering the full
Streams sampled in the riffle and leaf pack surveys
Map Locality Paluma
Kirrama
Mission Beach Tully Gorge Atherton Mt. Bellenden Kerr – Mt. Bartle Frere Malbon Thompson Range (Yarrabah)
Kuranda – Lamb Range
Black Mountain Mount Lewis Mossman/Mt. Carbine Mt. Windsor Daintree (Mount Thornton)
Lorna Doone (Far Northern)
Map ref. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36
Stream Name Keelbottom Little Crystal Birthday Camp Goddard Bridge Yuccabine Limbo Pixies Charappa North Johnson Nigger Bartle Frere Kearney Malbon Thompson Simmonds Oombunghi Kauri Breach Clohesy Shoteel Rifle Allan Windmill Mary Gorge Carbine Mt Windsor Oliver Emmagen Baird Bloomfield Woobadda Gap Wallaby Scrubby
Altitude (m a.s.l.)
Stream Order & Dominant Lithology
Survey sampled
600 400 800 850 500 100 600 20 60 620 500 900 1400 80 100 40 40 900 700 700 450 440 350 900 900 80 1175 960 20 20 200 20 100 150 300 140
3 (Granite) 3 (Granite-P) 3 (Granite-P) 2 (Granite) 3 (Granite) 3 (Granite) 3 (Granite) 3 (Alluvium/Met.)† 3 (Volcanics) 3 (Granite) 3 (Granite) 3 (Granite) 1 (?) 3 (Basalt/Granite)† 2 (Granite) 2 (Granite) 3 (Granite) 1 (Granite) 3 (Granite) 2 (Granite) 2 (Metam.) 3 (Metam.) 3 (Metam.) 2 (Granite) 2 (Granite) 2 (Hodgk./Granite)† 3 (Granite) 3 (Granite) 3 (Hodgk.) 4 (Hodgk.) 4 (Hodgk.) 4 (Hodgk.) 4 (Hodgk.) 2 (Granite) 2 (Alluvium) 3 (Granite)
R94 LP R93 & LP R93 & LP R93 R93 R93 R93 R93 & LP R93 R93 R94 R95 R94 R93 R93 R94 R93 R93 LP R93 & LP R93 R93 R93 & LP LP R94 R94 R94 LP R93 & LP R93 R93 R93 R93 R93 R94
† Requires on-site verification. Map locality and ref. refer to Fig. 1. Lithology: Granite P, porphyrytic granite; Hodgk., Hodgkinson granites and metamorphics, including siliceous cherts; Met., metamorphics. Survey sampled: R93, riffle survey 1993 (November – December); R94, riffle survey 1994 (May – July); R95, riffle survey 1995 (November); LP, leaf pack survey (August – September 1997).
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latitudinal and altitudinal range of the Wet Tropics; the second sampled the fauna of pool leaf packs from 10 streams.
METHODS Riffle survey: sampling and identification
The 36 Wet Tropics streams sampled in the riffle and leaf pack surveys are listed in Table 1, with their location plotted in Figure 1. Riffle-inhabiting chironomids were sampled from 32 of these sites over three years as part of a broader study of the region’s freshwater communities (Pearson in press). All streams flow through tropical rainforest and are characterized by very soft waters (hardness 1.8–21 mg/L) of low conductivity (22–111 S/cm) and variable but usually mildly acidic pH (5.5–6.8) (Butler & Pearson 1998). On the mountain peaks, annual mean air temperatures generally fall between 17 and 21C, but occasionally drop below zero in the winter. The coastal lowlands are warmer, especially in the north of the bioregion where the average annual mean temperature is often above 25C (Nix 1991). More southerly lowlands are a few degrees cooler, and regimes on the inland tablelands are similar to those of the mountain tops. Most sites (23) were sampled in the late dry season (November and December) of 1993 (R93, Table 1). The remaining sites, expanding altitudinal, latitudinal and seasonal coverage, were sampled in May and June 1994, following the end of the wet season, except for Bartle Frere (the highest mountain in the region at 1622 m a.s.l.), which was sampled in November 1995 (R94R95, Table 1). At each stream site, two riffles were sampled by thoroughly disturbing the substrate within six randomly placed 25 cm 25 cm quadrats (three per riffle) upstream of a dip net (63 m mesh), with collected material preserved in 70% ethanol. Because of the large number of larval chironomids found (approx. 7400), individuals were identified to species level from only two of the six samples collected per site, one per riffle. Abundance was highly clumped, with one or two samples from each site typically yielding many more individuals than the remainder, and so in each case the samples selected were those yielding the greatest number of individuals. These samples represented 57 9% (mean standard deviation) of individuals collected per site. Diversity was also well represented in these samples. For example, average richness per site was 71% of that found by Cranston (2000a), despite his samples integrating all habitats, and richness of the two samples for one stream (Birthday Creek, 17 species) was comparable to that assessed from six riffles intensively sampled as part of another study in
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1999 (19 species, BGM unpubl. data). Individuals were slide mounted in Hoyer’s aqueous solution and identified using the keys of Cranston (1997a,b, 2000b). Novel morphospecies with distinctive mouthpart morphologies were given a mnemonic (e.g. a number preceded by the letters ‘FNQ’ (Far North Queensland) for an undescribed putative genus). During the 1993 sampling trip, physico-chemical data were recorded from each site, as detailed in Butler and Pearson (1998). Methodology followed the Queensland ‘State of the Rivers’ pro-forma (Andersen 1993), and included measures of temperature, pH and conductivity, replicate measures (10) of width, depth and water flow over the stream reach sampled, as well as estimates of substrate composition and percent canopy cover (shading). By necessity, the exact time at which temperature measurements were taken varied among sites, but all were taken in the shade during daylight hours, and temperatures of Wet Tropics streams typically vary by less than two degrees over a 24-h period (B. G. McKie, P. Wulf and R. G. Pearson, unpubl. data, 2002).
Leaf-pack survey for chironomids of the Wet Tropics
As leaf packs support a different chironomid assemblage from riffles, a survey of this habitat from 10 streams was conducted in the 1997 dry season (August–September, Table 1), to broaden the understanding of the Wet Tropics fauna. Samples consisted of fist-sized handfuls (volume approximately 300 cm3) of leaves, collected from dense accumulations in slower-flowing pools, which were placed directly into a plastic bag containing 70% alcohol. Five separate leaf packs were sampled over a reach of approximately 100 m at each stream site. Chironomid larvae were identified as described above.
Biogeographical categorization
Where possible, species were allocated to biogeographical groupings comprising Gondwanan taxa, with recent postulated phylogenetic (sister group) linkages to other Gondwanan landmasses, and cosmopolitan taxa. Within the Gondwanan group, two subgroups can be recognized: cool, with current southern temperate distributions; and warm, with modern distributions in the warmer parts of the southern continents, often including tropical Africa. In contrast to these patterns, a cosmopolitan component comprises mostly broadly ranging taxa, both within Australia and elsewhere, with various relationships, some to proximate landmasses to the north,
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but without close phylogenetic association with Gondwanan landmasses.
Analysis
Distributional data were ordinated using Non-metric Multidimensional Scaling (NMS, Clarke 1993). Similarities in chironomid faunal composition among sites were assessed additionally using UPGMA (unweighted pair group arithmetic average) cluster analysis (Sneath & Sokal 1973). These analyses were conducted using the PC-ORD for Windows multivariate analysis package (Version 4.0 1999, MjM Software, Gleneden Beach, Oregon, USA). Additionally, an Analysis of Similarities (ANOSIM) was carried out using Primer for Windows (Version 5.2.9, 2002, Primer-E Ltd, Plymouth, UK) to assess differences between sites sampled in 1993 and 1994. Since the main interest was assessing similarities between sites, rather than groupings of samples within sites, data for the two riffle or five leaf pack samples (in the riffle and leaf pack surveys, respectively) from each site were pooled prior to analysis. All analyses used Bray-Curtis dissimilarities as the distance measure. Following ordination, simultaneous plots of streams and species in the ordination space were produced using PC-ORD. Scores for the species were calculated via weighted averaging, whereby stream unit scores are used to weight the average position of each species along the ordination axes. This allows for a visual assessment of relationships between species and sites, similar to a traditional principal components biplot, but
one which better accounts for non-linearity in these relationships (McCune & Mefford 1999). Riffle survey samples had been collected up to 7 years prior to identification, and some were poorly preserved. For three genera (the orthoclads Corynoneura and Thienemanniella and the Chironominae Tanytarsus), antennal characteristics crucial for species recognition were damaged. Therefore, data were pooled for two Corynoneura and two or three Thienemanniella species in the analyses. Two Tanytarsus species could be recognized from all sites, because characters important for species recognition were adequately preserved. Remaining Tanytarsus were excluded from analyses. These measures were unnecessary for the leaf-pack survey. Riffle survey data were additionally analysed using univariate regression, in order to assess relationships between species diversity and the altitude and latitude of the study sites. Standard measures of species diversity were used (evenness, species richness and the Shannon-Wiener, Simpson and Berger-Parker diversity indices), calculated using the Species Diversity & Richness program (Version 1.2, 1997, Pisces Conservation, Lymington, UK). In the riffle survey, assemblage composition appeared to be influenced by altitude (see Results below), and so univariate regression was used to explore relationships between altitude and stream physico-chemical characteristics. Where replicate measures were taken at each site (e.g. for depth, width and water flow), the response variable consisted of the average of the 10 readings. All regressions were carried out using SPSS for Windows (version 10.0.5, 1989–1999, SPSS Inc., Chicago, USA).
Fig. 2. Riffle Survey: results from NMS ordination (Bray-Curtis dissimilarities) of ln(x + 1) transformed chironomid abundance data. Ordination in three dimensions, axes 1 & 2 plotted; stress = 0.16. (a) Stream site coordinates, with altitude categories superimposed: () 19S, () 18–19S, () 17–17.99S, () 16S) and altitude (()
