Hiding in the background: community-level patterns in invertebrate herbivory across the tundra biome

In a paper recently published in Polar Biology, Sarah Rheubottom and collaborators investigate patterns of invertebrate herbivory across the tundra biome. Previous studies measuring invertebrate herbivory in tundra focused on a single host plant or a small group of species, but for the first time, in this study losses of plant tissue to invertebrate herbivores are assessed at the plant community level across a large number of tundra sites. The study also addressed how these patterns relate to long-term climatic conditions and the weather in the year of sampling, habitat characteristics, and aboveground biomass production.

Invertebrate herbivores depend on external temperature for growth and metabolism, so invertebrate herbivory is expected to increase as a result of continued warming in tundra ecosystems. The study found that invertebrate herbivory occurred low intensities but was present at all sites. On average <1% of the total plant community biomass was removed by invertebrate herbivores. The intensity of herbivory was influenced by mid-summer temperature, with warmer sites having greater leaf damage, but most of the variation in herbivory was associated with local ecological factors. More details about the local drivers of invertebrate herbivory are necessary to predict the consequences for rapidly changing tundra ecosystems.

Reference: Rheubottom, S.I., Barrio, I.C., Kozlov, M.V., Alatalo, J.M., Andersson, T., Asmus, A., Baubin, C., Brearley, F.Q., Egelkraut, D., Ehrich, D., Gauthier, G., Jónsdóttir, I.S., Konieczka, S., Lévesque, E., OLOFSSON, J., Prévey, J., Slevan-Tremblay, G., Sokolov, A., Sokolova, N., Sokovnina, S., Speed, J.D.M., Suominen, O., Zverev, V., Hik, D.S. (2019) Hiding in the background: community-level patterns in invertebrate herbivory across the tundra biome. Polar Biology (in press)

https://doi.org/10.1007/s00300-019-02568-3


Picture: Damage by leaf miner on Betula nana (photo: Isabel C Barrio, Agricultural University of Iceland, 2017)

Geese mediate vegetation state changes with parallel effects on N cycling that leave nutritional legacies for offspring

Roger Ruess and colleagues have just published a very interesting paper in Ecosphere, on vegetation shifts mediated by geese. You can read the abstract below.

Along the coastal fringe of the Yukon–Kuskokwim River Delta in southwestern Alaska, geese maintain grazing lawns dominated by a rhizomatous sedge that, when ungrazed, transitions to a taller, less palatable growth form that is taxonomically described as a different species. Nutrients recycled in goose feces, in conjunction with grazing, are critical to the rapid, nutritious growth of grazing lawns, and selective foraging on lawns has positive life-history consequences for goslings. To examine whether bidirectional vegetation shifts were accompanied by parallel changes in N cycling, we studied how 15N-urea and 13C15N-glycine were processed through soils and plants of native and recently reverted vegetation states. Biomass and plant 15N uptake from plots reverted to the tall growth form using exclosures and from those shifted to grazing lawns by experimental clipping and then goose grazing were identical to their native counterparts. Total recovery of 15N within the tall vegetation types was significantly greater than within grazing lawns, although when expressed on a per-gram biomass basis, percentage of 15N recovery was significantly higher in grazing lawns compared with the tall vegetation state. Patterns of 13C enrichment in CO2 soil efflux showed rapid use of 13C-glycine as a respiratory substrate within the first hour following injection, with both the timing and magnitude of efflux occurring at similar time points for all four vegetation types. However, higher soil respiration rates and a shorter half-life for 13C-glycine in soils from tall meadows resulted in a greater proportional loss of 13CO2 compared with grazing lawns. Despite daily to-weekly tidal inundation, all of 15N from labeled substrates could be accounted for within 1 m of the injection grid from soils of both states after 30 d, with significant levels of 15N in soils and vegetation after one year. Geese have remarkably high fidelity to brood-rearing areas, returning as adults to the same grazing lawns where they were raised as goslings. Our data suggest that the role fecal-derived nutrients play in the positive feedback loop between geese and their food resources can provide a long-term legacy that spans generations.

You can also access the full text of the article here.

Reference: Ruess RW, McFarland JW, Person B, Sedinger JS (2019) Geese mediate vegetation state changes with parallel effects on N cycling that leave nutritional legacies for offspring. Ecosphere 10(8):e02850


Picture: Pacific black brant (Branta bernicla nigricans)
(photo: Roger Ruess, University of Alaska)

Effects of reindeer grazing and recovery after cessation of grazing on the ground-dwelling spider assemblage in Finnish Lapland

The effect of reindeer grazing on the assemblage of ground-dwelling spiders was studied along the Finnish-Russian border fence on lichen dominated pine heath. Changes in species richness, abundance and evenness of spider assemblages were analyzed in relation to changes in vegetation and environmental factors in long term grazed and ungrazed sites, as well as sites that had recently switched from grazed to ungrazed and vice versa. Grazing was found to have a significant impact on height and biomass of lichens and other ground vegetation. However, it seemed not to have an impact on the total abundance of spiders. This is likely caused by opposing family and species level responses of spiders to the grazing regime. Lycosid numbers were highest in grazed and linyphiid numbers in ungrazed areas. Lycosidae species richness was highest in ungrazed areas whereas Linyphiidae richness showed no response to grazing. Four Linyphiidae, one Thomisidae and one Lycosidae species showed strong preference for specific treatments. Sites that had recovered from grazing for nine years and the sites that were grazed for the last nine years but were previously ungrazed resembled the long term grazed sites. In the long term ungrazed sites we found both spider and plant species typical of peatlands living among the thick Cladonia lichen mat on the sandy soil.

The results emphasize the importance of reindeer as a modifier of boreal forest ecosystems. The sites with reversed grazing treatment demonstrate that recovery from strong grazing pressure at these high latitudes is a slow process whereas reindeer can rapidly change the conditions in previously ungrazed sites similar to long term heavily grazed conditions.

You can read the full article here.

Reference: Saikkonen T, Vahtera V, Koponen S, Suominen O (2019) Effects of reindeer grazing and recovery after cessation of grazing on the ground-dwelling spider assemblage in Finnish Lapland. PeerJ 7:e7330 


Picture: Fence separating a grazed and an ungrazed site in Finnish Lapland (photo: Otso Suominen, University of Turku)

Amplification of plant volatile defence against insect herbivory in a warming Arctic tundra

Almost all plant species, particularly when stressed, release a complex blend of volatile organic compounds (VOCs) into the atmosphere. These VOCs are a fundamental defense of plants, conferring enhanced tolerance/resistance against abiotic stresses and acting as communication cues among community members. They also play important roles in atmospheric chemistry as they contribute to the formation of ozone and secondary organic aerosols.

Multitude of abiotic and biotic factors such as temperature and insect feeding are known to modulate the synthesis and release of plant VOCs. In the Arctic, however, no empirical studies have so far evaluated how climate warming and its concomitant increase in herbivory pressure interactively affect VOC emission patterns. In this study, we examined the effect of climate warming and increased insect activity on the release of plant VOCs to the atmosphere in the Arctic. We measured VOC emissions from dwarf birch Betula nana growing naturally in a subarctic wet heath, where ecosystem plots were subjected to passive warming by open-top chambers for 8 or 18 years.

The results showed that under 2°C of canopy warming obtained by open-top chambers, the plant leaf area consumed by insect herbivores increased by 300%. We exogenously applied a plant hormone methyl jasmonate to mimic plant defense responses to insect herbivory. We found that warming increased monoterpene emissions about twofold, irrespective of exposure duration, and that mimicked herbivory alone increase monoterpene emissions fourfold, and induced de novo synthesis and release of homoterpenes. Interestingly, combined warming and mimicked herbivory increased monoterpene emissions 11 fold, suggesting that warming amplifies the effects of herbivory on VOC emissions. 

Our observation of the unexpected high release rates of VOCs under combined warming and herbivory conditions suggest that increased insect activities will have a tremendous impact on VOC emissions in the Arctic and may tip into a domino effect on VOC-mediated interactions between species as well as the atmospheric chemistry. Our study underlines the importance of a focus on biotic stress on VOC emissions during climate change.

You can read the full paper here.

Reference: Li T, Holst T, Michelsen A, Rinnan R (2019) Amplification of plant volatile defence against insect herbivory in a warming Arctic tundra. Nature Plants 5:568–574


Picture: Assessing how climate warming and insect feeding affect plant volatile release from Arctic plants in Abisko, Sweden (photo: Riikka Rinnan, Copenhagen University).

The wild side: Norway’s herbivore communities are getting wilder

In many parts of the world, wild herbivores coexist with domestic livestock. Direct interactions between wild and domestic herbivores such as competition for forage often occur, as do indirect interactions such as apparent competition through predator densities. However, environmental management of wild herbivores and livestock is usually completely disconnected.

In a newly published paper, James Speed and colleagues analyse densities of wild herbivores and livestock in space (across Norway’s rangelands) and time (from 1949 to 2015). They find that livestock densities have greatly reduced, while wild cervids have increased in density. This is especially strong in milder regions, while mountain and northern regions remain dominated by livestock today (Figure 1).

Figure 1. Change in large herbivore communities across Norway from 1949 to 2015. Note the decline in the livestock assemblage and increase in forest cervids in the south east and central regions. The semi-domestic reindeer assemblage and mountain herbivore communities remain more stable over time.

These changes signify that Norway’s herbivore communities have become wilder – a process known as passive rewilding. However, both livestock and wild herbivores remain under stringent environmental management today. Interactions between wild and domestic herbivores, through both vegetation and predation, indicate that management of livestock and wild herbivores should be more integrated.

You can read the full paper here.

Reference: Speed JDM, Austrheim G, Kolstad AL, Solberg EJ (2019) Long-term changes in northern large-herbivore communities reveal differential rewilding rates in space and time. PLoS ONE 14(5): e0217166

https://doi.org/10.1371/journal.pone.0217166


Picture: Moose (Alces alces, European elk) is one of the species that has increased most in density across Norway from 1949 to 2015 (photo: James Speed, NTNU).

Can novel pest outbreaks drive ecosystem transitions in northern‐boreal birch forest?

Herbivores can sometimes alter the trajectory of entire ecosystems. In the northern-boreal mountain birch forest of Northern Fennoscandia, outbreaks by geometrid moths have caused mass mortality of mountain birch across large areas since the early 2000s. The severity of the outbreaks has been linked to the climatically facilitated range-expansion of the winter moth (Operophtera brumata), that has recently established itself as a new outbreaking defoliator in many areas that originally experienced outbreaks only by the native autumnal moth (Epirrita autumnata).

In the current study – focused on the Varanger region in northeast Norway – we show that the cumulative defoliation inflicted by such a novel two-species outbreak has exceeded a critical tolerance threshold (tipping point) of the forest, resulting in an abrupt increase in the mortality rate of birch stems. We also show that this severe mortality event has resulted in the loss of internal positive feedback mechanisms in forest regrowth, as regeneration by both basal sprouting and sapling production are positively affected by the presence of surviving stems and trees. Thus, reforestation may be very slow or fail altogether in areas that have been forced across critical tolerance thresholds and suffered mass mortality of trees. Accordingly, climatically induced alteration of moth defoliation regimes in the mountain birch forest could cause this ecosystem to undergo rapid and potentially persistent changes of state.

You can read the full paper here.

Reference: Vindstad, OPL, Jepsen, JU, Ek, M, Pepi, A, Ims, RA (2019) Can novel pest outbreaks drive ecosystem transitions in northern‐boreal birch forest? Journal of Ecology 107: 1141–1153.

https://doi.org/10.1111/1365-2745.13093


Picture: A conceptual model for how forest mortality induced by moth outbreaks may be followed by regeneration or a persistent transition to a treeless ecosystem state (photo: Jakob Iglhaut).

Reindeer grazing promotes plant phosphorus limitation in arctic tundra

Large mammalian herbivores occur in many terrestrial ecosystems and have large impacts on plant communities. They can for example change the availability of growth-limiting nutrients for plants, such as nitrogen (N) and phosphorus (P). Through this, herbivores might change nutrient limitation of plant growth (between N and P limitation) and thereby impact plant productivity.

Reindeer (or caribou) are important herbivores in arctic tundra and they are known to affect soil nutrient availabilities. In this study we examined the effect of long-term light and heavy reindeer grazing on nutrient limitation of plant growth in a Scandinavian arctic tundra. We performed a fertilization experiment, whereby we added N and P in a full-factorial manner, across the two grazing regimes in heath and meadow vegetation.

The productivity of the plant communities showed contrasting responses to our fertilization treatments under light and heavy reindeer grazing. Under light grazing, productivity increased with N and P additions in both the heath and meadow vegetation. Under heavy grazing, productivity increased when N was added in the heath, and increased even more when N was added together with P. In the meadow, productivity increased when P was added, either alone or in combination with N.

These results clearly show that heavy and long-term grazing by reindeer promoted P limitation of plant communities in both the heath and meadow vegetation. The mechanisms behind the shift towards these conditions were not the same in both vegetation types. In the N-poor heath, reindeer increased soil N availability due to a shift towards more N-rich graminoids, while in the meadow reindeer decreased soil P availability. It remains unclear how reindeer decrease soil P, but they may simply export more P from the system than N due to their large P demand for the production of their antlers.

In this study, we have experimentally confirmed that heavy grazing by large mammalian herbivores for a long time has the potential to change nutrient limitation of plant growth. Such a change can have significant ecological impacts, including changes in plant species composition and success of alien plant species.

You can read the article here.

Reference: Sitters, J., Cherif, M., Egelkraut, D., Giesler, R., Olofsson, J. (2019) Long‐term heavy reindeer grazing promotes plant phosphorus limitation in arctic tundra. Functional Ecology

https://doi.org/10.1111/1365-2435.13342


Picture: Herd of reindeer on the heavily grazed side of the fence in Reisadalen, Norway (photo: Judith Sitters)

Trophic interactions and abiotic factors drive functional and phylogenetic structure of vertebrate herbivore communities across the Arctic tundra biome

It is important to understand how biotic communities are organized, because that will determine how they respond to environmental changes. Beyond the number of species present in a community, two other aspects of diversity can provide useful information about the processes of community assembly. These aspects include how species are related to each other (phylogenetic diversity) and how similar they are in the ecological functions they perform (functional diversity).

In this study we investigate how different factors influence the phylogenetic and functional diversity of vertebrate herbivores across the Arctic tundra biome. We chose this group of organisms because herbivores play key ecological roles in tundra ecosystems. In turn, these ecosystems are likely to change substantially in response to the rapid environmental changes in this region. For example, ongoing warming and the northward expansion of boreal species could change the structure of herbivore communities in the Arctic. Further, Arctic vertebrate herbivore communities include species as functionally dissimilar as migratory, social grazers and solitary resident browsers, and as phylogenetically dissimilar as geese and ruminants.

We found that the functional and phylogenetic diversity of herbivore communities in the Arctic are driven by both bottom‐up and top‐down trophic interactions, as well as climatic severity. Under future warming and northward movement of predators, herbivore communities may become more phylogenetically and functionally diverse, with consequences to the functioning of tundra ecosystems.

Reference: Speed, J.D.M., Skjelbred, I.A., Barrio, I.C., Martin, M.D., Berteaux, D., Bueno, C.G., Christie, K.S., Forbes, B.F., Forbey, J., Fortin, D., Grytnes, J.A., Hoset, K.S., Lecomte, N., Marteinsdóttir, B., Mosbacher, J.B., Pedersen, A.O., Ravolainen, V., Rees, E.C., Skarin, A., Sokolova, N., Thornhill, A.H., Tombre, I., Soininen, E.M. (2019) Trophic interactions and abiotic factors drive functional and phylogenetic structure of vertebrate herbivore communities across the Arctic tundra biome. Ecography

https://doi.org/10.1111/ecog.04347

You can read the full article here.


Picture: An example of a phylogenetically diverse herbivore assemblage, with a Svalbard reindeer and a rock ptarmigan (photo: N. Lecomte, University of Moncton, 2019)

Biases in studies of spatial patterns in insect herbivory

Science is suffering a reproducibility crisis that is associated with the impacts of many biases on the outcomes of scientific research. Among these biases, those caused by the properties of the human mind are seldom appreciated by scientists working in the fields of ecology and environmental science. In the present paper, we asked to what extent studies of spatial patterns in insect herbivory suffer from various biases. We answered this question by comparing the outcomes of studies that have used methods of data collection which were potentially prone or not prone to particular biases. This comparison was conducted by meta-analysis of 125 scientific paper containing data on plant losses to insects in different environments. We found that biases emerged when scientists non-randomly selected one or a few plant species when assessing community-wide herbivory or when  scientists did not apply randomisation procedures when selecting leaves for measurements of herbivory. The reported effects were greater when the persons that collected samples and measured leaf damage were aware of the research hypothesis or sample origin than when the collectors/measurers were blinded to these factors. We conclude that our present-day knowledge regarding differences in insect herbivory between environments is considerably biased due to an unconscious tendency of researchers to find support for their hypotheses and expectations, as this generally leads to overestimation of the effects under study. These cognitive biases can be avoided by (i) applying randomisation procedures in sampling and (ii) blinding of the research hypotheses and sample origins. These measures should be seen as obligatory; otherwise, accumulation of biased results in primary studies can ultimately lead to false general conclusions in subsequent research syntheses.

Reference: Zvereva, E., Kozlov, M.V. (2019) Biases in studies of spatial patterns in insect herbivory. Ecological Monographs.

https://doi.org/10.1002/ecm.1361

You can read the full article here.


Picture: A tropical herbivore (bush cricket) mimicking leaf with insect damage (photo: V. Zverev, 2019)

Isotope ecology detects fine-scale variation in Svalbard reindeer diet: implications for monitoring herbivory in the changing Arctic

Svalbard reindeer females

In this study, Lily Zhao and colleagues use carbon and nitrogen stable isotope analysis to infer summer dietary differences of Svalbard reindeer found in different valleys. Through regression models, they were able to predict how reindeer dietary intake depend on climatic variables, with July temperature being the strongest predictor.  Using stable isotope analysis, they found robust dietary differences between and within reindeer populations separated by less than 50 km in the proportions of non-mycorrhizal vascular plants and mosses. These localized differences in forage availability related to the onset of the growing season as shown through the onset of the growing season in each valley through time. Overall, this publication provides evidence that carbon and nitrogen stable isotope analysis can detect dietary shifts over short time periods and at fine spatial scales, which means that isotopic studies can help monitor herbivory in the changing Arctic.

Reference: Zhao, L.Z., Colman, A.S., Irvine, R.J. et al. (2019) Isotope ecology detects fine-scale variation in Svalbard reindeer diet: implications for monitoring herbivory in the changing Arctic. Polar Biology.

https://doi.org/10.1007/s00300-019-02474-8

You can read the full article here.


Picture: Couple of Svalbard reindeer females and calf in April
(photo: Justin Irvine)