Researchers have revealed that declining plant diversity -- from habitat loss, human use, and other environmental pressures -- causes plants to flower earlier, and that the effects of diversity loss on the timing of flowering are similar in magnitude to the effects of global warming. The finding could have a powerful influence on the way scientists study ecosystem changes and measure the effects of global warming.

"Losing species from a system can shift the timing of biological events as much as climate change can," said Amelia Wolf, a postdoc in the Ecology, Evolution and Environmental Biology (E3B) department at Columbia University and lead author on the study. "Climate change has been shifting the timing of biological events such as flowering, raising concerns about timing mismatches between co-dependent species. This new paper is the first to demonstrate that, in addition to the impact of global warming, we need to be concerned about the ways that species losses are affecting the timing of biological events."

The paper, entitled "Flowering Phenology Shifts in Response to Biodiversity Loss," appears in the March issue of Proceedings of the National Academy of Sciences (PNAS).

Since the 1990s, farmers, naturalists and scientists have begun noticing that phenology, or the timing of biological events such as the flowering of plants and the "leafing-out" of trees, is changing, and plants have been flowering progressively earlier than they have in the past. To-date, this observation has been linked to rising temperatures resulting from global warming and, as such, flowering times have been described as a "fingerprint of climate change," understood as a public, visible, easily-measured display of the detrimental effects of global warming. As a result, numerous observational and experimental studies about the phenological impact of abiotic, physical influences -- like global warming -- have been conducted and published. There have not, however, been any studies that investigate the phenological impact of an ecosystem's biotic properties and the way living things interact with each other.

Additionally, there has been a disconnect between the data collected from observational studies, in which researchers observe and analyze what happens naturally in an ecosystem impacted by global warming, and results of experimental studies, where researchers artificially warm a plot in a way that matches natural global warming. The experimental studies consistently fail to produce the same changes to the timing of biological events as those recorded in observational studies.

"The experimental studies aren't able to account for all of the changes seen in the observational studies," Wolf said. "It's possible that part of what those experimental studies aren't able to account for is the biotic influence -- the impact of the other species surrounding those that are flowering. That would mean that it is not just global warming that is producing this effect, but there's a dual influence of changing temperature and changing species."

Wolf and her co-researchers set out to see if biodiversity loss had any effect on the timing of biological events. They created a grassland plot in California with 16 different species of plants, and systematically removed species to see what effect it would have on the remaining plants, an experiment that mimics human impact on the composition and diversity of plant communities worldwide. As they reduced plant diversity, the researchers observed warmer ground temperatures, changes in soil resources, and changes in flowering timing. For each species removed, remaining plants flowered, on average, about a half day earlier than they would in the absence of biodiversity loss. Two removed species resulted, on average, in plants flowering a full day earlier than they would otherwise.

The magnitude of this change in flowering timing, Wolf explained, is similar to the magnitude of phenological change previously attributed solely to global warming, which means that the role that biotic interactions -- how plants interact with each other -- have on phenology is critical to understanding the combined anthropogenic effects on leaf-out, flowering timing and other phenological events, and is something to be considered when studying global climate change. Declining diversity could be contributing to or exacerbating phenological changes attributed to rising global temperatures.

"This is not about when your tulips will reach full bloom, rather biodiversity loss and the impact it has on plant phenology can impact an entire ecosystem," Wolf said. "Plants flower to reproduce -- to create seeds to produce the next generation. A lot of plants rely on insects or birds or some other pollinator to help with this process. For such plants, changes in flowering time could be a really big problem. If a plant flowers before its pollinators are active, the plant species can't reproduce or may produce fewer seeds. If there are insects, birds, humans, or other animals that are dependent on those plant species, they could be influenced, as well. Plants and the communities in which they grow are interconnected and critically dependent on each other."

There are many ecological reasons why the timing of flowering matters, Wolf explained, and this new finding introduces a lot of new questions that need to be explored. This study, for example, was conducted in one type of ecosystem, but would researchers see similar patterns in other ecosystems? Wolf suspects they will. Among the other unknowns, the researchers are interested in analyzing which species are most likely to be affected by these biotic interactions; if there are species that are more insulated from the effects; and which species, if lost, result in the most significant changes in the community.