Biodiversity and Conservation (2006) 15:123–137 DOI 10.1007/s10531-004-4246-3
Associations between weevils (Coleoptera: Curculionidea) and plants, and conservation values in two tussock grasslands, Otago, New Zealand T.J. MURRAY1,*, K.J.M. DICKINSON2 and B.I.P. BARRATT3 1 Ensis, Private Bag 3020, Rotorua, New Zealand; 2Department of Botany, University of Otago, P.O. Box 56, Dunedin, New Zealand; 3AgResearch, Invermay Agricultural Centre, Private Bag 50034, Mosgiel, New Zealand; *Author for correspondence (e-mail: [email protected]
Received 5 January 2003; accepted in revised form 20 September 2004
Key words: Land conservation values, MDS, Plant–weevil associations, PRIMER, Tussock grassland invertebrates Abstract. Ecosystem level processes and species interactions have become important concepts in conservation and land management. Despite being New Zealand’s greatest contributors to global diversity, native invertebrates have been largely overlooked in the assessment of land values, and their diversity has often been assumed to reﬂect native plant diversity without justiﬁcation. Invertebrates can in fact aﬀect plant species composition, and in ecosystems such as New Zealand’s remaining indigenous and semi-modiﬁed tussock grasslands can do so in excess of more conspicuous vertebrate grazers. An understanding of the interactions between invertebrates and their plant hosts may be informative in assessing land conservation values, increase the eﬃciency of rapid inventory analyses and would be applicable across the production-conservation spectrum. This study considers the Curculionoidea, vascular plant, bryophyte and lichen communities of two semimodiﬁed tussock grasslands in the Otago region of southern New Zealand. Quantitative plant and invertebrate sampling were carried out in January 2001. Data were analysed using ANalysis Of SIMilarity (ANOSIM) and Multi-Dimensional Scaling (MDS) ordination techniques. Vascular plant, bryophyte and lichen species richness was highest in the same site and plots as native weevil species richness, however the proportion of native vegetation in these locations was lower. Associations identiﬁed between Curculionoidea and vascular plants were dismissed due to the confounding eﬀect of species frequency across samples. This appeared to have little inﬂuence on associations with bryophytes and/or lichens and these were given more weighting. The ecological implications of associations are considered and variability in weevil composition is discussed in reference to the tussock grassland environment. The importance of plant–invertebrate relationships to conservation and the uses and limitations of the PRIMER MDS ordination technique for determining associations are discussed.
Introduction Species interact both directly and indirectly through time and space. These interactions vary in form, frequency, intensity and complexity (Begon et al. 1990) and, in conjunction with abiotic factors, determine community structure and ecosystem function. Ecosystem and species interactions have become important concepts in sustainable management and conservation, as numbers of threatened species greatly outweigh conservation resources (Myers et al.
124 2000). By necessity therefore, biodiversity and ecosystem conservation are beginning to prevail over single species preservation (Ehrenfeld 2000), and previously overlooked organisms, like invertebrates, are beginning to receive greater consideration (McGuinness 2001). Land conservation values, which might include the presence of rare, not specialised or unique species and communities or high total biodiversity, are frequently assessed using methods which assume that native invertebrate diversity reﬂects native plant diversity. Although such correlations have been demonstrated (Moeed and Meads 1985; Crisp et al. 1998; Harris and Burns 2000) there has been little evaluation of this as a general principle. In fact, although generally characterised by their respective plant communities, the diﬀerential grazing of phytophagous invertebrates can also aﬀect plant-species composition (Patrick 1994) and even equal or exceed that of more conspicuous vertebrate grazers in, for example, tussock grasslands (White 1978; Andersen and Lonsdale 1990; Schowalter 2000). Nevertheless, there is pressure in ecological studies to use such methods which include ‘rapid inventory techniques‘ because they are comparatively cheap and quick (Crisp et al. 1998). Understanding relationships between invertebrates and their host plants may increase the eﬃciency of rapid inventory techniques by allowing more accurate predictions of invertebrate community composition to be made from botanical information which is often already available or more easily collected. For example, in the case of host speciﬁc herbivores, for which the host plant has been determined, the absence of that plant can be informative. Furthermore, knowledge of the ecology of particular invertebrates could be useful in the assessment of ecosystem health by understanding trophic structure, identifying the causes of ecosystem degradation, or increasing the success of restoration attempts. Invertebrates are New Zealand’s major contributors to global diversity with less than 2% of species having been introduced (Patrick 1994) and endemism reaching approximately 96% (Watt 1975). The Otago region of southern New Zealand has a particularly diverse invertebrate fauna and is thought to represent a major centre of invertebrate endemism (Barratt and Patrick 1987; Barratt and Kuschel 1996). A signiﬁcant proportion of this diversity occurs in the tussock grasslands characterising much of the montane inland areas. Although extensive, these areas are under-represented in Otago reserves (Allan 1978) and this is often due to their semi-modiﬁed ﬂoristic state with little regard for the invertebrate communities. During a collaborative study by the Department of Conservation, New Zealand Forest Research Institute and Landcare Research Limited assessing the eﬀects of ﬁre on tussock-grassland ecosystems, spatial disparities in adult weevil communities (Coleoptera: Curculionidae) were noted (Barratt et al. 2003; Murray et al. 2003). This paper sets out to further analyse these disparities by relating them to the vegetation characteristics at each site and plot, in terms of species richness and percent native species, as such data are often more readily available and used to determine the conservation value of a site.
125 We also investigate potential weevil-plant and weevil-bryophyte/lichen species associations using PRIMER, a novel method of multidimensional scaling ordination designed speciﬁcally for examining community structure (Clark and Warwick 1994). This statistically ﬂexible method is increasingly being used to analyse aquatic invertebrate communities (see Clarke 1993) but less widely in terrestrial settings.
Methods Study sites Sampling was conducted at Mt. Benger (4535¢ S, 16915¢ E) and Deep Stream (452¢10¢¢ S, 17015¢50¢¢ E), in mid-January 2001. Both sites represent seminatural Chionochloa rigida (Raoul) Zotov (1963) tall tussock grasslands with a diverse inter-tussock ﬂora. They have a recent history of low density stocking (Gitay et al. 1992; Ross et al. 1997) and have remained un-burnt for at least 25 years. The Mt. Benger (MB) site is situated on the eastern slopes of the Old Man Range at 1167 m a.s.l., and Deep Stream (DS) at 500 m a.s.l., 10 km north of Lake Mahinerangi (see Murray et al. 2003). This study utilises three 20 m · 20 m plots at each site giving a total of 6 plots, MB1, MB2, MB3, DS1, DS2 and DS3.
Sampling A quantitative measure of vascular plant and weevil species abundance was achieved by removing 20 intact 0.1 m2 inter-tussock turves (32 cm · 32 cm · 5 cm deep) per plot in a stratiﬁed design avoiding large Aciphylla plants and woody shrubs. Four additional turves per plot were taken to included tussocks (Chionochloa rigida) clipped to 100 mm above ground level. Individual turves were stored in paper sacks at 4 C until they were examined to determine the local shoot frequency of vascular plant species (following the nomenclature of Allan Herbarium 2000) with the aid of a 25-cell grid placed over the turf surface. The presence/absence of bryophyte and lichen taxa were recorded and identiﬁed following the nomenclature of Beever et al. (1992) for mosses, Glenny (1998) for liverworts, and Galloway (1985) and Martin and Child (1972) for lichens. Invertebrates were then collected by inverting whole turves and placing them individually in extraction funnels along with any material that may have come loose in storage or during vegetation recording. Turves were heated for 7 days by 150 W light bulbs mounted 400 mm above each turf and invertebrates were collected into 90% ethanol:10% glycerol. Curculionoidea were hand-separated from other invertebrates and stored in 70% ethanol. Bremner (1988) determined that between 97 and 100% of weevils present in a turf are recovered
126 using these methods, and that cool-storage of turves for up to 3 weeks has no negative eﬀect on this yield. Abundance of each weevil species/morpho-species, as identiﬁed by comparison to a reference collection held at AgResearch Invermay Agricultural Centre, was recorded per turf. Nomenclature follows Alonso-Zarazaga and Lyal (1999).
Analysis Non-metric Multi-Dimensional Scaling (MDS) sample ordinations (Kruskal and Wish 1978; Clarke and Warwick 1998) using the computer package PRIMER (Clarke and Warwick 1994) were employed to compare species compositions of each plot and site. Analysis of similarity (ANOSIM) permutation tests, which calculate the similarity coeﬃcient R, were used to tests the null hypothesis of ‘no diﬀerence’ in community composition between sites and plots, providing statistical support for the primarily visual interpretation of these ordination results. Species ordinations were performed to identify potential ecological associations between weevils and vegetative taxa as taxa occurring frequently in the same samples appeared close together on these graphs. Analyses were based on similarity matrices produced using the Bray– Curtis similarity measure (Bray and Curtis 1957) to deﬁne a similarity coeﬃcient between every pair of species (species ordinations) or turves (sample ordinations) and their varying abundances across all samples. All ordinations were run using one thousand iterations and were repeated multiple times. Abundance data were subject to 4th root transformation before ordination, to increase the weighting given to less common species while retaining abundance information. The resulting ordination graphs lack axes, instead each point, corresponding to a species or the composition of a turf in species and sample ordinations respectively, is placed in 2-dimensional space such that the relative distances between points match, in rank order, the corresponding pairwise similarities. The stress value indicates the adequacy of these distances (Clarke 1993), tending towards zero where the rank orders reach perfect agreement.
Results Community composition Mt. Benger supported greater species richness for all three taxonomic groups (Table 1) and almost twice the number of species recorded in only that site as opposed to in both sites. Vegetative species richness (vascular plants, bryophytes and lichens) was highest at Mt. Benger, however, the proportion of native vegetative species was slightly lower. Species richness was reasonably consistent between plots for all three groups at Deep Stream, as were the
127 Table 1. Number of vascular plants, bryophytes/lichens and weevil species collected in January 2001 at Mt. Benger (MB) and Deep Stream (DS). Values in parentheses indicate the number of species which are New Zealand native. The total proportion of vegetative species (vascular, bryophytes and lichens) that were native at each site and plot is also shown. Total number of species unique to each site and plot, in the context of this study is indicated. Site/plot
Bryophytes and lichens
Native vegetation (%)
MB DS MB1 MB2 MB3 DS1 DS2 DS3
57(44) 50(39) 38(27) 27(21) 40(29) 39(27) 36(27) 36(26)
32(22) 29(22) 14(10) 16(12) 20(13) 17(14) 17(14) 17(13)
17(17) 9(9) 8(8) 7(7) 16(16) 6(6) 7(7) 8(8)
74 77 71 77 70 73 77 74
39 21 14 12 28 12 10 13
number of native species recorded, but varied considerably more between plots at Mt. Benger. Weevil species richness was twice as high in plot MB3 compared to both MB1 and MB2. Although the total number of native vascular, bryophyte and lichen species was also higher in MB3, the proportion of native vegetation was lower at 70%. Those plots with the highest proportion of native vegetation (MB2 and DS2) exhibited two of the lowest scores for both total unique species (those not recorded in at least one other plot) and weevil species richness. MDS sample ordinations clearly indicated that the two sites diﬀered in their species composition for all three taxonomic groups (Figure 1a, c, e) and this is supported by the associated ANOSIM R-values displayed in Table 2. All plots can be clearly separated based on the vascular plant ordination (Figure 1b), however, plots MB1 and MB2 showed a high degree of overlap between sample points for weevils and also bryophytes and lichens (Figure 1d, f) which is reﬂected in the non-signiﬁcant R-values for these comparisons. The bryophyte and lichen species present at DS2 and DS3 were not suﬃciently diﬀerent (Figure 1d) to distinguish between the communities in these 2 plots.
Vascular plant–weevil associations An ordination of weevil and vascular plant abundance data from both sites indicated several instances where weevil and vascular plant species (or groups of species) frequently occurred in the same samples (Figure 2a). These particular associations, however, were not consistently evident in repeated species ordinations, or ordinations of each site independently, despite the low stress value (0.15) and high number of iterations. When the percentage of turves in which each weevil and plant species occurred was superimposed onto the
Figure 1. MDS sample ordinations of vascular plants, bryophytes/lichens and Curculionidae at the site (a, c, e) and plot (b, d, f) levels. Each point represents the species composition of an individual turf. (a, c, e) mMt. Benger; . Deep Stream; (b, d, f) m MB1; . MB2; n MB3; r DS1; d DS2; + DS3; n = number of turf samples.
ordination (Figure 2b) a pattern emerged. Generally, distances between species declined from the periphery to the centre of the ordination while the frequency of turves in which species occurred increased. Visual interpretation of repeated analyses indicated that each species remained at approximately the same position on this gradient from centre to periphery, however, at any point along this gradient directly adjacent species varied considerably from one repetition to the next, suggesting the potential associations in Figure 2a were an aberration of species frequency rather than representative of true associations between species.
129 Table 2. ANOSIM R-values and their associated signiﬁcance for between-site and between plot diﬀerences in weevil, vascular plant and bryophyte/lichen community compositions (species presence and abundance) at Mt. Benger (MB) and Deep Stream (DS). Signiﬁcance levels