Biodivers Conserv (2013) 22:905–919 DOI 10.1007/s10531-013-0457-9 ORIGINAL PAPER Non-geographic collecting biases in herbarium specimens of Australian daisies (Asteraceae) Alexander N. Schmidt-Lebuhn • Nunzio J. Knerr • Michael Kessler Received: 22 October 2012 / Accepted: 15 February 2013 / Published online: 21 February 2013 Ó Springer Science+Business Media Dordrecht 2013 Abstract Biological collections are increasingly becoming databased and available for novel types of study. A possible limitation of these data, which has the potential to confound analyses based on them, is their biased composition due to non-random and opportunistic collecting efforts. While geographic biases are comparatively well studied and understood, very little attention has been directed at other potential biases. We used Asteraceae specimen data from Australia’s Virtual Herbarium to test for over- and under- representation of plants with specific morphology, phenology and status by comparing observed numbers of specimens against a null distribution of simulated collections. Strong collecting biases could be demonstrated against introduced plants, plants with green or brown inflorescences, and very small plants. Specimens belonging to species with very restricted areas of distribution were also found to be strongly underrepresented. A mod- erate bias was observed against plants flowering in summer. While spiny plants have been collected only about half as often as should be expected, much of this bias was due to nearly all of them also being introduced (thistles). When introduced species were analyzed alone, a negative effect of spines remained but was much more moderate. The effect of woody or herbaceous habit, other inflorescence colours, tall growth and size of the capitula was comparatively negligible. Our results indicate that care should be taken when relying on specimen databases or the herbaria themselves for studies examining phenology, resource availability for pollinators, or the distribution and abundance of exotic species, and that researchers should be aware of collecting biases against small and unattractively coloured plants. Electronic supplementary material The online version of this article (doi:10.1007/s10531-013-0457-9) contains supplementary material, which is available to authorized users. A. N. Schmidt-Lebuhn (&) Á N. J. Knerr CSIRO Plant Industry/Centre for Australian National Biodiversity Research, P O Box 1600, Canberra, ACT 2601, Australia e-mail: [email protected] M. Kessler Institute of Systematic Botany, University of Zurich, Zollikerstrasse 107, 8008 Zurich, Switzerland 123 906 Biodivers Conserv (2013) 22:905–919 Keywords Asteraceae Á Australia Á Biodiversity databases Á Collecting bias Á Compositae Á Invasive plants Introduction Specimen data from natural history collections are increasingly available in online databases and enable innovative ecological, evolutionary, spatial and conservationist studies, espe- cially when combined with environmental or phylogenetic data (Graham et al. 2004). However, these studies may be confounded by two major problems of the underlying data, taxonomic inaccuracies or misidentifications (Graham et al. 2004) and a skewed composition of biodiversity collections resulting from biased or opportunistic collecting activity. The most intensively researched forms of collecting bias are geographic in nature. Biodiversity collections of various groups of organisms have been demonstrated to be biased towards readily accessible areas (Williams et al. 2002; Reddy and Davalos 2003; Sanchez-Fernandez et al. 2008), especially roadsides (Kadmon et al. 2003), towards areas attractive for their status as nature reserves or the occurrence of specific habitats (Sanchez- Fernandez et al. 2008) and towards specific climatic zones (Loiselle et al. 2008). These biases have the potential to make biodiversity databases less useful than they seem and to distort the inference of environmental niches or of centres of diversity (Nelson et al. 1990; Tobler et al. 2007; Hortal et al. 2008; Soria and Kessler 2008), but at least they are comparably well known and understood, and are thus more easily taken into account. Non-geographic collecting biases, especially those connected with intrinsic character- istics of individual species, have received much less attention, although it can reasonably be assumed that they also have the potential to distort the results of scientific studies relying on specimen databases or, more directly, those utilizing only the specimens themselves. In fact, even explicit hypotheses have rarely been formulated. Guralnick and Van Cleve (2005) suggested that rare species, in their case birds, may be collected more frequently than common species. In contrast, Williams et al. (2002) suspected that rare species were more likely to be missed, but also that small species would likely be underrepresented in collections. Gonzalez-Oroczo et al. (2012) compared diversity scores resulting from analyses using generalist collections and targeted specialist sampling for germplasm collections but found only minor differences. Zopfi (1993) remarked that, compared with field observations, large specimens of the herbaceous plant genus Rhinanthus were underrepresented in herbaria, presumably because botanists prefer to collect individuals that would fit nicely onto a herbarium sheet. Specifically for plants, some other hypotheses readily suggest themselves: Collectors might be expected to have a preference for showy plants as opposed to those with a subdued floral display, and to avoid spiny, thorny, prickly or urticating plants, or species that are fertile during unpleasantly hot, rainy or cold seasons. Hypotheses like these have, unfortunately, generally not been tested quantitatively. We therefore decided to use an existing specimen dataset to examine several potential collector biases. The Asteraceae (daisy family) are an ideal group to examine such biases due to their large species number, wide distribution and ease of recognition despite a large morpho- logical diversity including spiny and unarmed species, diverse flower colours, a wide range of capitulum sizes and diverse forms of habit and life cycle (Fig. 1). The major Australian herbaria have databased their collections of vascular plants and made them available in a readily accessible online database, so that data on species-specific collecting activity is 123 Biodivers Conserv (2013) 22:905–919 907 Fig. 1 Photographs illustrating the morphological diversity of Asteraceae found in Australia and some of the characters potentially subject to collecting biases. a Large and shrubby Ozothamnus ledifolius, b tiny annual Angianthus micropodioides, c colourful native ornamental Rhodanthe chlorocephala, d inconspic- uously brown-flowering Euchiton sphaericus, e Microseris lanceolata, a native species superficially similar to weedy dandelion and showing the very common yellow flower colour, and f introduced and spiny Cirsium vulgare 123 908 Biodivers Conserv (2013) 22:905–919 available for the entire continent. The following hypotheses about collector biases in Australian Asteraceae were tested in this study, with the null hypothesis in all cases that there is no significant effect of the examined trait: (1) Introduced plants are underrepresented. It is assumed that the majority of collectors is interested in studying the native flora. (2) Spiny plants are underrepresented. It is assumed that they are more unpleasant to collect. (3) Plants with attractive or rare colour schemes are overrepresented. Yellow is an extremely common colour in Asteraceae, and this has even prompted the creation of the acronym DYC for ‘‘Darn Yellow Composites’’. It is assumed that more colourful or unusually coloured species will be collected more often than those characterized by plainer or more frequent colours. (4) Species flowering in the Australian summer, here defined as December to February, are underrepresented. It is assumed that many collectors avoid conducting field work in the most oppressive heat. (5) Very small species are underrepresented in collections. It is assumed that they will be overlooked more easily and that they are bothersome to collect because several plants are needed to fill one herbarium sheet. (6) Very large herbaceous species are underrepresented. It is assumed that many collectors have been trained to collect herbaceous plants with roots, and that they will hesitate to collect plants that do not fit onto a herbarium sheet in their entirety. (7) Species with large capitula or large glomerules (compound capitula) are overrepresented. It is assumed that they are more attractive and conspicuous to most collectors. (8) Although not a collecting bias, we also tested one hypothesis related to area size, that species with small areas of distribution (local endemics) are underrepresented relative to their area of distribution. It is assumed that they are on average locally rarer than widespread species (Gaston and Blackburn 2000). Materials and methods Datasets Morphological and phenological information was obtained from regional floras and tax- onomic revisions (Curtis 1963; Lander and Barry 1980; Dunlop 1981a, b; Jessop 1981; Burbidge 1982; Short 1983a, b, 1985 1987,1989, 1990a, b, Short 1995, 2000a, b; Cooke, 1986; Wilson 1989; Brown 1992; Holzapfel 1994; Hunger 1996; Jeanes 1999; Walsh 1999; Keighery 2002; Wheeler et al. 2002; Thompson 2004a, b, c, 2005a, b, 2006; Walsh 2007; Wilson 2008a, b; CANBR 2010). The following characters were coded: native or intro-