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Instituto Pirenaico de Ecología (CSIC)

Secrets of some of the Pyrenees’ threatened plants

Here the author takes us on a tour of the results obtained over the last two decades of field studies on four Pyrenean species listed in Aragon’s Catalogue of Threatened Species (CEAA): Pinguicula longifolia subsp. longifolia, Petrocoptis pseudoviscosa, Cypripedium calceolus and Borderea chouardii.

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 As everyone knows, plants are primary producers and underlie ecosystems’ biodiversity. We depend on them for the oxygen we breathe, our food and many other goods and services we humans, and all other living creatures in the food chain, enjoy. Over the last decade, however, we have been HIGHLIGHTSProfile: María Begoña García
bombarded with gloomy predictions of a drastic and rapid loss of global biodiver­sity, based on ecological niche models and future scenarios of climate change. This pessim­istic vision is based on a single non-experimental methodology, which has not always been confirmed by the, al­beit scant, recent studies monitoring plants over the last few decades. If the predictions for the most common plants are not promising, it is logical to suppose that they will be worse still for threatened species. We therefore need to under­stand the role of these rare plants in the ecosystem and determine their real vulnerability to the global changes taking place.

This article sets out the results obtained over the last two decades of field studies on four Pyrenean species listed in Aragon’s Catalogue of Threatened Species (CEAA): Pinguicula longifolia subsp. longifolia, Petrocoptis pseudoviscosa, Cypripedium calceolus and Borderea chouardii (Figure 1). They are just a few examples, but they illustrate the living history of plants with extremely limited distributions.

These random examples allow us to look from a different and more objective angle at their ecology and population dynamics, so as to better understand the keys to their existence today and propose more effective measures to avoid their future loss.

Figure 1. Aspect of the four plants discussed (left to right, top to bottom): Pinguicula longifolla subsp. longifolla, Petrocoptis pseudoviscosa, Cypnpedium calceolus and Borderea chouardii. / Photos courtesy of the author.

We will start with Pinguicula longifolia subsp. longifolia (Lentibulariaceae), a plant endemic to the central Pyrenees catalogued as being of “special interest.” It is a rupicolous butterwort (a type of carnivorous plant) with leaves up to 30cm long that hang over the damp limestone rocks it lives on, creating sticky passive traps for passing insects. As with many other plants, its flowers are visited by pollenisers (mainly long-proboscis hymenoptera and dipterous insects), thanks to which it bears fruit and numerous tiny seeds able to reach new “ecological islands” where they can germinate. Unlike many other plants, however, they also take advantage of these insects This humble, rare, long-leafed Pyrenean butterwort is the basis of a rich network of biotic interactionsby catching them in their leaves and killing them. Most of the arthropods between 1 - 4 cm that approach the plant are trapped when they come into contact with the specialised glands on their leaves. The insects are digested for their nutrients by enzymes secreted by tiny sessile glands. The young leaves are in contact with the limestone rock face when they start to develop, and their prey are accessible to other creatures that collect them as if they were shopping for food: the ants that swarm around on the damp rock. However, this butterwort’s traps are not able to catch large flying insects such as crane flies and butterflies, nor the smallest arthropods which are also common in their environment: mites in the group Oribatula tibialis which stroll around underneath the penduncular glands as if they were on a stroll through a beech wood. This tiny mite (a subspecies new to science which has not yet been described and does not seem to be found anywhere else) feeds on the remains of the butterwort’s prey once they have been digested by its leaves (Figure 2) and it lives in the nooks and crannies formed by the revolute leaves, where they shed their skins, excrete, and we have also observed pregnant females. It is quite possible that this interaction is beneficial for the plant as the mite feeds on hyphae and fungi that may represent a threat to it.

Thus, this humble and rare long-leafed Pyrenean butterwort, which, like many other carnivorous plants, inhabits nutrient-poor sites, is the basis of a rich network of biotic interactions: not only symbiosis such as pollination and the possible benefit of a unique mite that only lives on its leaves, but other inter­actions in which there are losers: its carnivorous feeding habits and the ants’ cleptobiosis of its prey. The decline or loss of this catalogued plant would entail the loss of another important type of diversity in a delicate and unrepeatable microcosmos: that of a dense and exclusive network of interactions that has evolved over millions of years.

The next story relates to a plant catalogued by the CEEA as “vulnerable” as it lives in just one valley in the Aragonese Pyrenees: Petrocoptis pseudoviscosa (Caryophyllaceae).

Like the previous plant, this is also a rupicolous plant living in inaccessible locations. P pseudoviscosa is distributed in five populations of very different sizes: from just a hundred or so to several thousand. This situation allows us to test the widespread idea that small populations are more prone to extinction than large ones. To do so hundreds of plants in three populations were monitored individually. This made it possible to estimate characteristic vital rates of each of them (survival, growth, fertility, etc.), factor them in to stochastic matrix models and evaluate the extinction rate over a 100 year horizon using classical population viability analysis (Figure 3).

Figure 2. Prey captured by the leaves of Pinguicula longifolia subsp. longifolia. The arrow shows the position of two mites (Oribatula tibialis) feeding on the prey after its nutrients have been digested by the plant’s leaves. / Photo courtesy of the author.

The population that turned out to be the most stable, and therefore at least risk of extinction, was neither the largest nor the smallest. We would not have reached this conclusion if we had worked on the data in isolation from the population structure (that which had the lowest ratio relative to reproducers, The fact that there are organisms so well adapted to living in the poorest places on earth will never cease to amaze uswhich could lead us to consider it senescent), seed germination (the lowest), and fruit predation (the highest). Only by a combination, integrating all the vital cycle rates, are we able to characterise current functioning and make predictions about the future based on real empirical data. The key to understanding the difference in population behaviour in this case lies in the average age of the larger adults, which is in the range of 18 to 50 years. Further studies also showed that the species is not just self-compatible (i.e. it can form seeds fertilised with its own pollen), but that the seeds produced in this way germin­ate as well as those obtained by cross-fertilisation. This possibility undoubtedly gives plants living in “ecological islands” considerable autonomy, as they need to develop mechanisms to ensure individual’s survival after colonising new enclaves.

Let’s leave rocky habitats for a moment to look at rich pastureland and the woodland margins of the central Pyrenees, where four populations of Cypripedium calceolus, a beautiful orchid known as “lady’s slipper,” present in numerous European countries, are found. It is catalogued as “endangered” in the CEAA as its distribution is limited to the SW Pyrenees.

Reports at European level consider it to be in serious decline, having disappeared from at least one EU country. Studying it in the Pyrenees allowed us to test the paradigm that peripheral populations are in a worse state than central ones. This could also give us an idea of how more than a hundred vascular woodland plants with Eurosiberian affinities in the absolute southernmost limit of their distribution are functioning. With this goal, dozens of groups and hundreds of individual plants were monitored over ten years.

Figure 3. Schematic representation of a plant’s generic life cycle, showing the transition between size classes and the various factors that can intervene. This type of information is used at the basis of population viability analysis.

Interestingly, none of the parameters analysed was worse in the Pyrenean populations than the central ones: population sizes were similar, average fruiting was much higher, and the population growth rate matched or exceeded that shown in data from other European countries. And again, the stochastic matrix models tell us that the risk of extinction over the next century is nil. The peripheral Pyrenean populations do not respond to theoretical expectations. It is therefore worth asking what is behind this unexpectedly benign situation today, given that the Pyrenees are slowly becoming warmer. The oldest retrospective There are no “good” or “bad” processes in nature, just reorganisations of energy and diversityimages available for popu­lations fifty years ago can help us understand why this rare plant is not currently faring any worse than it used to. In the wake of the gradual abandonment of traditional uses of mountain areas, the places where the lady’s-slipper orchid grow have grad­ually become covered in trees and bushes, which has almost certainly changed populations’ microclimates. Whereas the average temperature in the Pyrenees has risen, orchid populations have probably been kept cooler by the increased shade. This is an example of how local changes can be much more important than global ones. There are no “good” or “bad” processes in nature. There is simply a re­organisation of energy and diversity. And there are always winners and losers. The recovery of the woodlands means the loss of the diversity that has built up in the meadows. But it also stabilises the soil, stores water and biomass resources, and improves the conditions for its associated species.

Let’s go back to the harsh rocky habitat to explore one of the most fascinating of plant stories, that of Borderea chouardii (Dioscoreaceae). This tiny dioecious geophyte, a living fossil from the tertiary period, was discovered in the 1950s and lives exclusively in the cracks of a limestone crag in the Aragonese Pyrenees. It is catalogued by the CEAA as “endangered” and is a priority plant in the European Union Habitats Directive (1992), having been the object of the first recovery plan officially promoted in Spain (1994). Since then, having overcome the difficulty accessing it by setting up a scaffolding and working in uncomfortable locations, hundreds of plants have been monitored individually, and this has enabled us to discover the unusual reproductive secrets and dynamics of this unique species. As in the case of R pseudoviscosa and C. calceolus most of the studies conducted began thanks to a LIFE project obtained in 1996 by the Aragonese regional government, which has con­tinued its support for this line of work to the present.

The first visual estimate of the population suggested a figure of between 300 and 500 plants. This was later increased to 9,000 by means of searches with binoculars and telescopes, and more accurate surveys of its in­accessible terrain. During this period it was also possible to bolster the population by sowing seeds in cracks and founding new populations, which are now producing their first reproductive individuals.

Figure 4. Borderea chouardii tuber over 200 years old. The red spots mark some of the scars left by its annual stems. / Photo courtesy of the author.

The first surprise the plant gave us was that it is possible to determine its age, as like its congener B. pyrenaica it has the peculiarity that the annual stem leaves a small scar on the outside of the tuber. Using the dead tubers trapped in the cracks it was possible to determine the age of a handful of plants, with the surprising result that they were over 300 years old. Given the small size of the tubers, and the fact that they do not reproduce by vegetative propagation, it is possible that we have come across the slowest growing plant in the world (Figure 4).

The next surprise came with the study of their population dynamics: we knew that there were few small plants in the population, so we feared that this was an extremely old population in decline. However, the matrix models of population dynamics show year after year that the population cannot be considered to be shrinking but is stable. The projection for the population 500 years in the future is very similar to today’s. For a plant that originated millions of years ago, and has survived various glaciations, our 17 years of monitoring have been but the blinking of an eye in its long evolutionary history. We have to humbly admit that despite the fact that although the detailed time series data that we have collected on this plant rate among the longest in the world, in fact it may still be insufficient to fully understand the plant.

The third surprise this unique plant gave us was its reproductive system. From the start of ecological monitoring we frequently observed that the few new seedlings on the rock face in each annual census were isolated and remote from the nearest potential mother plant, even though this species uses the typical mechanism We have learned from these plants that rarity is not the same than as being endangered, just one of the ways of livingmany rupicolous plants use for seed dispersal: the recently fertilised flower turns to insert the ovary in a nearby crack, where the seeds develop and are released when the fruit dries. How did the seeds reach these inaccessible locations? A painstaking study of its habitat over several years, watching somewhere were nothing ever seems to happen, revealed that it is ants that pollinate its flowers and disperse its seeds. Two different genera of ants are involved in the essential process of sexual reproduction in order to maintain the population, despite the fact that ants have generally been considered nectar thieves rather than effective pollin­ators, and here are barely a handful of cases in the world where their dual role as pollin­ators and dispersers have been shown. When founding new populations, therefore, the existence of ants able to move pollen and seeds has to be considered to ensure the future success of the species.

The secrets we have extracted from these four “threatened” plants are just a sample of the many that remain to be discovered among rare mountain plants. The fact that there are organisms so well adapted to living in the poorest places on earth, such as cracks in the rock face, where they nevertheless manage to maintain a stable population, will never cease to amaze us. We have learned from these plants that rarity is not the same than as being endangered, just a way of living. While we discuss their situation of danger, they, tougher than the rocks they live on, look down in amazement...

Profile: María Begoña García

María Begoña García is a CSIC staff scientist at the Instituto Pirenaico de Ecología [Pyreneen Institute of Ecology] (CSIC). She obtained her doctorate in sciences (Biology), in 1993 from the Instituto Pirenaico de Ecología (CSIC), on the reproduction and demographics of endemic plants in the Pyrenees, with grant funding from the Government of Aragón. After taking her PhD, she spent two years in Sweden and New Zealand, four years at the Doñana Biological Station (reincorporation contract) and two years at the University of Seville (Ramón y Cajal). She has taught at the universities of Navarre, Zaragoza, Seville, and Pablo de Olavide (Seville). Her current research line is on the dynamics and conservation of biodiversity at the community level (spatial patterns on altitude gradients, assembly rules, and changes in recent decades) and species populations (trends and analysis of population viability in rare, threatened and indicator plants, and plants at the limits of their distribution).

Published in No. 09

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  • Lychnos. ISSN: 2171-6463 (Spanish print edition),
    2172-0207 (English print edition), 2174-5102 (online edition)
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