Biases in estimation of insect herbivory from herbarium specimens

Abstract

information regarding plant damage by insects in the past is essential to explore impacts of climate change on herbivory. We asked whether insect herbivory measured from herbarium specimens reflects the levels of herbivory occurring in nature at the time of herbarium sampling. We compared herbivory measurements between herbarium specimens collected by botany students and ecological samples collected simultaneously by the authors by a method that minimized unconscious biases, and asked herbarium curators to select one of two plant specimens, which differed in leaf damage, for their collections. Both collectors and curators generally preferred specimens with lesser leaf damage, but the strength of this preference varied among persons. In addition, the differences in measured leaf damage between ecological samples and herbarium specimens varied among plant species and increased with the increase in field herbivory. Consequently, leaf damage in herbarium specimens did not correlate with the actual level of herbivory. We conclude that studies of herbarium specimens produce biased information on past levels of herbivory, because leaf damage measured from herbarium specimens not only underestimates field herbivory, but it is not proportional to the level of damage occurring in nature due to multiple factors that cannot be controlled in data analysis.

Changes in plant collection practices from the 16th to 21st centuries: implications for the use of herbarium specimens in global change research

“…However, contrary to expectations, we did not discover any temporal shift in the aesthetic value of herbarium specimens. This finding suggests that, as in the case of selectivity with respect to insect damage ( Kozlov et al , 2020 ), the importance of aesthetic reasons varied among collectors, and this variation appeared much greater than the temporal shift in the importance of aesthetic reasons in the selection and preparation of herbarium specimens. The importance of aesthetic reasons can also depend on external circumstances and would be lower in specimens collected during short-term excursions to remote localities than in specimens sampled next to a botanist’s home.…”

“…The substantial increase in the number of leaves in herbarium specimens between 1558 and 2016 may also have affected the levels of insect herbivory measured from these specimens. Botanists have always been advised to collect specimens that bear no or few signs of damage ( Greville, 1840 ; Bailey, 1899 ; Pearsall, 2015 ), and an earlier study demonstrated that both collectors and curators generally preferred specimens with less leaf damage ( Kozlov et al , 2020 ). Obviously, finding a large (50‒100 leaves) branch with no or minor leaf damage is more challenging than selecting a small (5‒15 leaves) branch with no traces of insect feeding.…”

“…Herbarium use, in particular, has diversified during the past century ( Heberling et al , 2019 ), and some scientists are calling for a more intensive utilization of these ‘windows into the past’ in global change research ( Meineke and Davies, 2018 ; Meineke et al ., 2018 , 2019 ; Lang et al , 2019 ). However, plants preserved in herbaria do not constitute a random sample from a population ( Kozlov et al , 2020 ); therefore, we cannot exclude the possibility that the temporal changes observed in the characteristics of herbarium specimens do not reflect solely the changes in biota. Rather, these changes may also mirror shifts in plant collection practices.…”

“…For example, some plants, such as the lianas of the genus Mikania , are represented in herbaria almost exclusively by their very tips, whereas lower leaves are rarely sampled even though they often differ markedly from upper leaves ( Holmes, 1993 ). A recent study showed that insect herbivory measurements obtained from leaves of herbarium specimens are not proportional to the level of herbivory occurring in nature ( Kozlov et al , 2020 ). Some biases associated with the use of herbarium specimens can be moderated while searching for ecological patterns ( Delisle et al , 2003 ; Fithian et al , 2015 ), but the number of studies accounting for these biases remains relatively low.…”

Response to Kozlovet al.: Inaccurate estimation of biases in herbarium specimen data

“… Summary Kozlov and colleagues 1 call into question the application of herbarium specimens to quantify historical patterns of herbivory 2–5 . It is already widely appreciated that collectors of herbarium specimens may tend to avoid insect damage, thus making herbivory estimates from herbarium specimens potentially down-biased 2 .…”