In a paper published in Ecological Monographs in 1996, Sarah Hobbie reported the results of her laboratory experiments on the effect of increased temperature and species composition on litter decomposition in the Alaskan Tundra. Hobbie found that increased temperature led to “increased rates of soil and litter respiration, litter decomposition, litter nitrogen release, and soil net nitrogen mineralization”. At the same time differences in these parameters between certain pairs of species were sometimes larger than the differences for the same species in two temperature treatments. Hobbie’s findings suggested that global warming could thus affect litter decomposition in the Alaskan Tundra both directly and indirectly (through changes in species abundance). Twenty-two years after the paper was published, I asked Sarah Hobbie about the origins of her interest in this topic, her memories of conducting this study, and what we have learnt since about this topic.
Citation: Hobbie, S. E. (1996). Temperature and plant species control over litter decomposition in Alaskan tundra. Ecological Monographs, 66(4), 503-522.
Date of interview: Questions sent by email on 5th January 2018; responses received by email on 16th August 2018.
Hari Sridhar: This paper is based on work you did during your PhD at UC Berkeley. Could you set this paper in the context of the rest of your PhD and tell us what the motivation for this specific piece of work was?
Sarah Hobbie: As a PhD student, I became interested in how individual species could have ecosystem-level impacts – how species might differ sufficiently that they could have divergent effects on processes like decomposition and nutrient cycling. But in the tundra, because plants grow so slowly and the system is highly sensitive to disturbance because of permafrost, it’s difficult to manipulate the abundances of species to compare their individual effects. Species removals are possible, but take a long time to have effects, and planting monocultures or otherwise manipulating abundances is basically impossible. Therefore, the only feasible way to examine species effects on decomposition and nutrient cycling that I could think of was to establish microcosms, where I could measure decomposition and simultaneously measure the soil nutrient cycling consequences of different species litter decomposition. I was also interested in how large the differences among species might be compared to the direct effect of warming, in the context of climate change. For example, might the effects of warming, operating through changing species abundances, be as or more important than the direct effects of warming on these processes?
HS: Stepping back a bit, how did you get interested in the arctic ecosystem and the topic of nutrient cycling?
SH: When I was a senior in high school, I was fortunate to travel to the Canadian Arctic on a 40-day canoe trip as part of program run by a wilderness camp in Northern Minnesota. I later became a trip leader for this camp, and led high school seniors on two other long canoe trips to arctic Canada. Something about that northern, wide-open, treeless landscape really captured me. I was always interested in biology, and when I finally decided to study ecology (I was also considering adolescent medicine and biochemistry), it occurred to me that it would be fascinating to actually study that landscape that I felt so drawn to.
As I learned more about the ecology of the Arctic, I came to appreciate the importance of climate change and nutrient cycling in the Arctic. Nutrients are a strong constraint over the productivity of tundra ecosystems and are a significant manifestation of the short growing seasons and cold temperatures of high-latitude, permafrost systems, and thus their availability is likely to change as climate warms.
HS: If you don’t mind my asking, why wasn’t your PhD supervisor an author on this paper?
SH: Two reasons. First, these ideas were largely ones that I came up with. Second, my PhD advisor, Terry Chapin, is quite generous about authorship issues – he will not include himself if he doubts at all that he should be included. It’s hard for me to assess, in hindsight, whether, given my current perspectives on authorship, I would consider that he was being overly generous in that regard for this particular paper. I just can’t remember well enough.
HS: Could you give us a sense of what a typical day of fieldwork was like during this study – where did you stay, how did you commute, did you have help during fieldwork etc.? When you think back to this time, what are your most striking memories?
SH: I did much of this study in the laboratory back at the University of California, Berkeley, but in order to carry out the experiment, I had to collect litter and soils from Toolik Lake, Alaska. Collecting litter and soils in arctic tundra is very different from collecting them in any other sort of ecosystem. The plants I was collecting were tiny, and I needed to collect dead stems, recently senesced leaf litter, and roots. I had to devise different methods of collecting material for each species. The species I remember best was Vaccinium vitis-idaea, or lingonberry, a dwarf shrub. Its leaves are tiny, about half a centimeter long. The species is evergreen and when the leaves senesce, which happens throughout the summer, they remain on the tiny branches. To collect them, I had to lie on the tundra and use a tweezers to gently tug at senesced leaves, one by one. I only collected those that had clearly abscised, so that they easily came free from the branch. Often they would fall at the touch of my tweezers, so I would try to retrieve the fallen leaves from in between the mosses and lichens. I remember spending days lying on the ground collecting leaf litter. I think I listened to a Walkman to pass the time. Much of the time I wore bright yellow rain gear, because the ground is very wet in the tundra since the permafrost impedes drainage. I recall that the folks in camp at the Toolik Research Station could see me across the lake, essentially motionless on the ground, and they couldn’t figure out why I appeared to be lying still in the tundra for hours on end. I had to use tiny scissors to trim dead branch tips for the same species. I collected senesced leaf litter of the sedge species the same way, since these species’ leaves senesce from the tips of the blades downward to the base. I felt like I was giving the Eriophorum vaginatum tussocks a haircut, as I trimmed individual blades to separate senesced from live tissue. Separating roots from peat is a pain in the neck because the only way to do it is to carefully pull the peat away from the roots. The Ericaceous species have such fine roots that it took a long time to get sufficient mass to carry out the experiment. So all in all, it was a pretty tedious process. Fortunately, I did have some help from some field assistants and my advisor, and a postdoc who was working at the station was able to collect leaf litter from the one deciduous shrub, which changed color and dropped its leaves after I had to leave the station for the summer.
HS: Some of the lab work was done at the Centre for Water and the Environment of the University of Minnesota. How did this collaboration come about?
SH: I didn’t have the capabilities to measure litter carbon fractions at Berkeley, but I knew that they did at the University of Minnesota, Duluth, from their publications. So I contacted them and asked if they’d be able to conduct those analyses for me. Fortunately, they were able to do that on a fee for service basis.
HS: You say “Frozen soils were then shipped back to the University of California, Berkeley.” How exactly did you do this?
SH: I placed blocks of frozen peat into large coolers, and then shipped them from Fairbanks.
HS: When was the last time you visited Toolik Lake? Do you still work there? How has it changed since the time you worked there for this study?
SH: Unfortunately, I haven’t been back to Toolik Lake since 2002, when my last grant to work there ended. I shifted my research focus for two primary reasons. First, I had kids, and wanted research sites closer to home so that I wouldn’t have to be gone for such long periods of time when my kids were young. Second, it’s very expensive to work at Toolik, because of the logistics costs (the flights are expensive and the daily user fees are quite high). It thought it would be easier to help students fund their research if we didn’t have to worry about covering the high logistics costs.
I certainly miss it, and I hear that it’s changed considerably since I was there. When I worked there we didn’t have showers – we relied on the sauna to get clean – and many of us chose to sleep in tents, as opposed to staying in trailers. Many of the facilities have grown in size – labs, sleeping quarters, dining facilities – and there are now showers.
HS: You acknowledge a number of people at the end of your paper. Could you tell us a little more about who they were, how you knew them and their contribution to this paper:
- Chris Lund – Chris was a summer research assistant for me and my advisor. He was an undergraduate at Carleton College and he helped me collect litter and soil.
- Megan McGlinchey – Megan was also a summer research assistant with us who helped collect litter and soil.
- Terry Chapin – Terry was my graduate advisor.
- Loretta Johnson – Loretta was a postdoc working at Toolik with Gus Shaver who helped me collect Betula nana leaf litter at the end of the season, after I’d had to leave the station.
- Eleanor Zhou – Eleanor was an undergraduate at UC Berkeley who helped me with lab work.
- Hailin Zhong – Hailin was Terry’s lab manager at UC Berkeley who helped me with lab work.
- Brad Dewey – Brad was John Pastor’s lab manager at the University of Minnesota, Duluth, who carried out the carbon fraction analyses.
- John Pastor – John was a professor at the University of Minnesota, Duluth, whose lab carried out the carbon fraction analyses.
- Carla D’Antonio – Carla was a member of my dissertation committee who gave me feedback on a draft of the manuscript (which was also a dissertation chapter).
- David Valentine – Dave was a reviewer of the paper.
HS: How long did the writing of this paper take? When and where did you do most of the writing?
SH: Oh gosh, I can’t remember these details.
HS: Did this paper have a relatively smooth ride through peer-review? Was Ecological Monographs the first place this was submitted to?
SH: My best recollection is that the review process was relatively smooth. Ecological Monographs was the first place I submitted it.
HS: What kind of attention did this paper receive when it was published?
SH: In those days, it was a bit hard to know, because we didn’t have “impact factors” or twitter or other kinds of social media. In fact, we barely had email! So, I don’t really know that much about how it was received, except that I have been surprised over the years by how often it is cited, I guess because it was a lab study instead of a field study.
HS: What kind of impact did this paper have on your career? In what ways, if any, did it influence the future course of your research?
SH: I’m still interested in how individual species influence ecosystem processes, including carbon and nutrient cycling, and have done a number of studies that are directly related to this one. For example, I conducted a follow-up study at Toolik in the early 2000s where I decomposed litter of the dominant species from two different landscapes that differed in time since glaciation, and therefore in a number of soil properties and in their vegetation composition. I was interested in how the vegetation might be resulting in feedbacks to soil processes. Later, I conducted several studies in a replicated common garden of different tree species in Poland. We’ve had a number papers come out examining the influence of these different tree species on carbon and nutrient cycling in litter and soil. Currently, I have an ongoing decomposition study in a network of long-term nutrient addition experiments, where we are using a reciprocal transplant design to study the effects of nutrient enrichment on decomposition, teasing apart the direct effects of nutrient enrichment from effects occurring through changes in the plant community. And finally, I’ve been studying how trees affect land-water transfer of nutrients and contribute to storm-water pollution in cities, as leaf litter decomposes in the street gutter.
HS: Today, 21 years after it was published, would you say that the main conclusion still holds true, more-or-less: “This experiment indicates that future climate warming will alter C and N cycling through a number of mechanisms. First, warming will directly stimulate rates of C and N cycling through litter and soil. How- ever, substrate quality also limits rates of litter decomposition and N release. This study adds to the growing evidence (e.g., Pastor and Post 1988) that changes in plant community composition as well as changes in plant allocation will be just as important as direct warming effects in determining future C and N cycling.”
SH: Yes, I would say that the conclusions regarding changes in plant composition hold true, and that our confidence in those conclusions has grown. For example, a meta-analysis of decomposition studies that was led by Will Cornwell (Cornwell et al. 2008) led to the same conclusion – the differences in decomposition rates among different species are large relative to the differences among sites caused by climate differences. Cross-site studies and meta-analyses of root versus leaf litter decomposition have also revealed systematic differences between their rates of decomposition, although I would say that we still don’t know that much about how climate change will alter the relatively productivity and turnover of root versus leaf litter, particularly for the finest order roots that turnover most rapidly.
HS: If you were to redo this study today, what would you do differently?
SH: I would have loved to have conducted this experiment in the field, but I can’t figure out to this day how I would have done that.
Since doing this study, I’ve gained an appreciation for the importance of other aspects of litter chemistry in influencing decomposition (particularly Ca and Mn, and more recently phenolics and tannins), so I probably would have measured more aspects of litter chemistry. I’ve also become a bit more sophisticated about how I approach fitting decomposition models to data, so I might have tried fitting different exponential decay models and added another time point to be able to distinguish better among different models in their ability to describe the data. We’re also learning a lot recently about important differences among root orders in their decomposition rates (Goebel et al. 2011, Sun et al. 2016), but I honestly can’t imagine isolating the lower orders of these roots, particularly for the ericaceous species, to examine their decomposition separately. I just don’t think it would have been feasible.
HS: You say “Differences in decomposition rate among different litter types (leaf, stem, and root) were as great as differences within a litter type between the two temperature treatments. Therefore, changes in allocation among plant organs in response to climate change will have large effects on decomposition. Allocation changes more with nutrient addition than with manipulation of other resources (light, water) or conditions (temperature, Parsons et al. 1994, Chapin and Shaver 1996). Thus, allocation will probably respond more to changes in nutrient availability resulting from climate change than directly to climate change. Species generally respond to increased nutrient availability with greater shoot allocation (Tilman 1988). Indeed, nutrient addition increases aboveground biomass relatively more than belowground biomass in tundra (Chapin and Shaver 1996). However, species differ in whether they respond to nutrient addition with greater leaf or stem allocation (Parsons et al. 1994), with large implications for feedbacks to decomposition. Future research should thus focus on generalizing the consequences of climate change for allocation.”
To what extent has research along the lines of your suggestion happened? What do we know today about the effects of climate change on allocation?
SH: Unfortunately, we know more about the patterns of biomass distributions across broad scale climate gradients than we do about patterns of allocation, likely because it’s such a pain in the neck to measure belowground NPP. For example, analyses of large global data sets for forests show that proportional biomass of roots relative to foliage increases as temperatures decline (Reich et al. 2014). However, a more recent analysis of a global NPP data set did not find that allocation patterns to NPP were related to aspects of climate (Chen et al. submitted; [published]).
These data sets come from forests and it is difficult to know whether such patterns hold in non-forested biomes. In particular, tundra remains understudied compared to other biomes with regard to root production (Iversen et al. 2015). Thus, how climate change affects allocation in tundra ecosystems remains unresolved.
HS: You say “This study adds to the growing evidence that net nitrification may occur in tundra soils, although rates are low relative to rates of ammonification (Fig: 8) (Nadelhoffer et al. 1992). As shown previously in tundra soils (Chapin et al. 1988), warming significantly increased net nitrification. The increase in net nitrification with warming probably resulted from both direct temperature stimulation of nitrification (Paul and Clark 1989) as well as from greater NH4+ availability in the -warmer incubations. Whether net nitrification will increase with warming under field conditions where plant roots may compete with nitrifiers for NH4+ is unknown.”
Do we know more about the how warming affects net nitrification today?
SH: A recent study showed a high amount of diversity of ammonia oxidizing archaea in arctic tundra soils, suggesting high potential for nitrification in field conditions; and high gross rates of nitrification and large increases in ammonium consumption and nitrite production warming soils from 4 to 20°C (Eloy Alves et al. 2013) in laboratory incubations. Interestingly, in that study, rates declined from 20 to 28°C. Another recent study showed that plants in arctic tundra take up nitrate at rates comparable to plants in warmer climates (Liu et al. 2018). These findings don’t directly address your question about warming effects, but they do point to the importance of nitrification and nitrate nutrition in arctic tundra.
HS: You say “Because of the long-lived nature of woody stems, effects on decomposition will likely lag behind production responses of woody shrubs to climate change. However, predicting such lag times is hampered by our lack of knowledge regarding mortality of woody stems.”
Do we know more about mortality of woody stems today?
SH: My perusal of the literature suggests that we are making progress in understanding variation in mortality of plants in arid ecosystems in response to drought, but I don’t know that much progress has been made in determining causes of mortality in arctic tundra.
HS: You say “Past warming in the Arctic and sub-Arctic has been associated with C accumulation. For example, peat formation occurred in Beringia during the Boutellier Interval, a period of warming 40 000 yr ago between the mid-Wisconsin Happy and the late-Wisconsin Duvanny Yar intervals (Hopkins et al. 1982). Early- to mid-Holocene warming was associated with faster rates of C accumulation in many Arctic sites and with the onset of peat development in sub-Arctic Canada (Ovenden 1990, Marion and Oechel 1993). However, why warming increased C accumulation and peat development is unknown. In light of this study, the role of warming- induced vegetation change in altering decomposition and promoting C storage should be determined.”
To what extent has research along these lines happened?
SH: Indeed, there has been a great deal of research addressing (1) how recent warming has affected shrub growth and abundance in the Arctic, and (2) what the consequences of increased shrub abundance are for net energy and carbon balance. In fact, there has been enough research in this area that it’s challenging to summarize it here (it would be a good topic for a review paper!). This has been a major focus of research throughout the past two decades.
HS: Have you ever read this paper after it was published? If yes, in what context?
SH: I’ve glanced at the paper from time to time, mostly to remind myself of the results, as I have a terrible memory! I’m still struck by the slow decomposition of the mosses, and I’ve looked back at the paper to see whether patterns revealed in other papers, such as slower decomposition of roots relative to leaf litter (Freschet et al. 2013), were evident in this study (they were not).
HS: Would you count this paper as a favourite, among all the papers you have written?
SH: I do like a few things about this paper, and I look back on it fondly. First, it was one of the first papers to consider and compare decomposition of different plant organs (roots, stems, leaves) across species. And the conclusions regarding species differences would have been different if I had only considered leaf litter. As a scientific community, we still measure leaf litter much more commonly than we measure decomposition of wood and roots, even though roots and wood are important components of NPP. Second, it was important in showing how slowly mosses decompose relative to other species and also that because mosses are poor carbon substrates for soil microorganisms, they influence nitrogen cycling in ways that might not be expected. This gave me new appreciation for the importance of peatlands for storing carbon and also led me to learn about crazy things like “bog men”, the preserved men that have been pulled from Sphagnum bogs in northern Europe. Third, I think this paper has been important in helping people think about how the increased “shrubbiness” of tundra that has been observed with climate warming in experiments, long-term observations, and the paleoecological record might alter soil carbon and nutrient cycling. So, I guess it is among my favorites!
HS: What would you say to a student who is about to read this paper today? What should he or she take away from this paper written 16 years ago? Would you point him or her to other papers they should read along with this paper? Would you add any caveats?
SH: I think we are learning a lot about how plant species influence carbon and nutrient cycling in soils in ways that are not necessarily related to litter decomposition, or are related to litter decomposition in ways that we haven’t always appreciated. So, I would caution students to think more broadly about how plant species can influence soil processes, and to pay attention to the evolving notions of soil organic matter formation and dynamics. In addition, it’s clear that tundra species can influence nutrient cycling through mechanisms that do not involve litter decomposition (e.g., by influencing the soil physical environment by altering snowpack). I would also caution students that our understanding of root decomposition is rapidly increasing as we learn more about variation in decomposition among different root orders.