Natural succession as a restoration tool ― Editorial

Ecosystems are continuously being serverely damaged by human activities, and we are now beginning to understand that these changes often disrupt ecological processes that we rely on.  Thus ecological restoration is becoming increasingly critical.  Practitioners of ecological restoration often use technical means, including the use of heavy machinery and large amounts of manual labor, to restore biodiversity to damaged areas.  This is often very expensive; nevertheless we must find a way to rehabilitate the overwhelmingly large amount of damaged ecosystems throughout the world.

In ecological restoration we are concerned with increasing the natural value of degraded areas.  Apart from technical restoration, changes within ecosystems occur through natural succession.  Often a primary goal in restoration is to increase the cover- and diversity of vegetion.  One doesn't expect to see these increases, at least not through natural succession alone, at sites which are extremely toxic or dry.  However, one could use technical restoration methods until the plant community becomes capable of continuing the succession process on its own.  On steep slopes, or other areas where the threat of landslides or erosion is great, re-vegetating the site as quickly as possible is clearly justafiable; and faster formation of continuous vegetation cover is a common advantage of technical restoration methods.  A study looking at erosion in Fujian Province, China, indicated that 20 % vegetation cover represents a restoration threshold, beyond which natural succession can be embraced.

A number of scientific investigations by Czech biologists suggest that leaving Czech post-mining sites to undergo natural succession can be beneficial for aquatic- and terrestrial communities.  Amphibians benefit from natural succession in these areas, as this process creates many small shallow ponds, rich in vegetation, throughout the landscape; while sites which are reclaimed by technical methods are typically flattened and contain only large deep ponds which are vegetated only within the riparian zone, and contain predatory fish.  Sites where natural succession prevails often represent various stages of succession, called seral stages; and landscape-scale studies have indicated that a greater diversity of seral stages tends to increase regional biodiversity.

Strategically embracing natural succession as a restoration tool can save time, money, and effort, and lead to more-diverse ecosystem development.  At many sites, technical measures may be necessary to prevent- or remediate extreme environmental damage.  Of course, there are countless degraded sites at which biodiversity can re-develop from natural succession alone.  At countless other sites we can surely find a balance between technical restoration methods and the strategic use of natural succession; this balance would be specific to the restoration site in question.  A limited-intervention approach has been suggested for wide use.  This limited-intervention approach involves assessing limiting factors for a particular site's development, leading to a restoration approach using the minimum effort required to meet specific restoration goals.  Additionally, as long-term monitoring remains one of the largest let-downs in conservation science- and practice, this approach may help the field move forward by allowing more-robust monitoring efforts due to the money saved on restoration methods.  Considering the amount of terrestrial- and aquatic habitat that currently requires restoration, the limited-intervention approach may be the wisest and most feasible option.

Arctic marine mammal conservation

Earth's marine mammals are disproportionately threatened compared to land mammals, and the 11 species of arctic marine mammals (hereafter AMMs) are particularly threatened due to their dependence on sea ice.  Some AMMs require sea ice for certain activities (e.g. reproduction, feeding, resting), while other use ice but are not dependent on it.  AMMs refer to species that occur north of the arctic circle (66° 33' N) for most of the year, as well as some species that seasonally inhabit arctic waters.  AMMs include 3 whales (narwhal, beluga, and bowhead); 7 pinnipeds (ringed, bearded, spotted, ribbon, harp, and hooded seals, and walrus); and the polar bear.  Throughout much of their range, these animals are important nutritional resources for indigenous people.  Recent research indicates that the greatest species richness of AMMs is in the atlantic regions of Baffin Bay, Davis Strait, and the Barents Sea (figure 1); while the lowest species richness was found in the Sea of Okhotsk and the Beaufort Sea.

Figure 1:  Geographic regions of the arctic marine ecosystem.

Warming in the arctic over the past several decades has been about 2 times greater than the global average, and scientists predict an ice-free arctic in summer by 2040.  Of the 12 arctic marine regions, 11 show significant trends (1979-2003) toward earlier spring sea-ice melting, later autumn sea-ice formation, and thus longer summers (figure 2).  Only the Bering Sea showed no trend.  The trend was most extreme in the Barents Sea.  The trend of sea-ice loss is surely guaranteed for at least the next several decades, regardless of global efforts to reduce greenhouse-gas emissions.

Figure 2:  Trends (1979-2013) in length of summer season (time from spring sea-ice melt to autumn sea-ice formation).

In addition to declining sea ice surface area, the thickness of sea ice has greatly decreased.  Continuation of this thinning is expected to further effect summer ice extent, as storms and other weather anomalies substantially impact thin ice.  Loss of sea ice has affected survival in some polar bear populations.  The survival of pinniped pups is impacted by the melting of sea ice because the young need sufficient time for suckling.  Snow depth (which has been decreasing in the arctic) directly affects whether ringed seals can construct lairs on the sea ice.  Additionally, loss of sea ice habitat will affect the ability for indigenous people to harvest AMMs because much of the hunting occurs on the sea ice or near the ice edge.

Climate change has widespread ecological implications for the arctic, yet the effects are under-reported despite changes exceeding those of temperate, tropical, and mountain ecosystems.  This is partly due to logistical challenges in assessing marine mammal populations in the arctic, due to wide distributions, cryptic behavior, and the remoteness of marine areas.  Population data are important for understanding conservation priorities, but estimates for most AMM populations are lacking.  AMMs are highly mobile, seasonally moving long distances, across regional- or international boundaries.  Thus management requires international collaboration.  Given the fast pace of these changes in the arctic, and the uncertainty in how AMM populations will respond, flexible- and adaptive management will be critical.

It is necessary to understand- and mitigate the impacts from industrial activities.  Longer open-water seasons are contributing to increased use of shorter international shipping routes.  Potential threats associated with oil- and gas development include underwater sound and oil spills.  International agreements may be needed to protect AMM habitats of high importance, especially those of industrial interest.

It is critical that all stakeholders recognize AMMs as organisms with innate value, and as resources connected to the well-being of the indigenous people who harvest, interact, and live with them.  Accurate scientific data will be central to making informed- and effective conservation decisions.

LINK to Laidre et al.'s 2015 article in Conservation Biology.

Owl population restoration in Luxembourg

Central European cultural landscapes used to be mosaics of meadows, orchards, hedgerows, fields, and forests.  Unfortunately, most of these landscapes have been recently homogenized and converted to monocultures.  This process has been a typical result of agricultural intensification.  In the second half of the 20th century, this homogenization has further increased due to land being used to grow plant resources for producing "green energy" such as biofuel and biogas.  The intensification of farming techniques such as the use of inorganic fertilizers and pesticides, and the conversion of diverse landscapes into intensive monocultures, has resulted in widespread severe population declines for a variety of different animal groups.  Local- and country-specific management actions are being implemented to prevent further losses of farmland birds.  For successful conservation, measures need to include actions like hedgrow provision to improve the feeding and breeding habitats of farmland birds.  However, conservation measures vary between species, thus for effective species conservation we must consider species-specific habitat requirements.

The little owl (Athene noctua) is a nocturnal raptor.  It is a small owl, usually 22 cm tall with a wingspan of 56 cm, and weighing about 180 g.  The core of its distribution is located in the temperate steppes and deserts of the Mediterranean region, including north- and northeast Africa; but it inhabits much of the temperate and warmer parts of Europe, and Asia eastward to Korea (figure 1).  This bird uses meadows, grasslands, and fields for hunting, and it nests in trees.  The destruction of forests, and the conversion of these ecosystems to open agricultural land allowed A. noctua to colonize major parts of central Europe.  Today, it often nests in old trees of high-stem orchards, and in buildings and quarries with suitable cavities.  But A. noctua populations have severely declined throughout Europe in recent decades, and the species is now red-listed in several European countries.  Local conservation measures have included the installation of nesting boxes in potentially-suitable habitats, preferrably in high-stem orchards.

Figure 1:  Geographical distribution of the little owl (Athene noctua).

In Luxembourg, A. noctua is near extinction.  85% of Luxembourg's land surface is agriculture and forest, and in recent decades there have been strong increases in agricultural intensification, livestock, and urban expansion.  These landscape changes have resulted in the loss of shrubs and trees; and this loss in landscape- and habitat diversity has led to the loss of many arthropods and small mammals, these being the main food sources for A. noctua.  Inventories of breeding pairs of A. noctua in Luxembourg during recent decades shows a severe population decline:  In 1960, there was an estimated 4200 breeding pairs; but only 15 to 20 breeding pairs existed in 2002.  To prevent further population collapse, 450 nesting boxes were installed since 1999 in major parts of Luxembourg.

63 study sites in high-stem orchards were randomly selected.  The presence- or absence of A. noctua at nesting boxes was recorded for each study site, and the distance to the next settlement was measured.  Presence/absence was assessed during the mating season (march and april) by using audio recordings of male territory calls, invoking responses from other members of the species.

28 of the 63 study sites (27 of the 38 sites with nesting boxes) were occupied by A. noctua in 2012.  The probability of A. noctua presence was much higher at sites with nesting boxes than sites without nesting boxes.  This pattern was consistent across the entire study region, and proximity to other A. noctua breeding pairs had no detectable effect on presence/absence of the species; this further suggests that, in Luxembourg, nesting-site availability is the limiting factor for this species.  The high relevance of nesting boxes for conservation was also seen in studies in Germany, where about 90% of all A. noctua pairs were breeding in artificial nesting boxes.  Originally, old trees in high-stem orchards, as well as old buildings, provided important nesting sites.  However, these structures have largely vanished in today's landscapes.  It should be noted that, for many species, nesting-site availability has been shown to be crucial for maintaining populations.  A combination of fields suitable for hunting and nesting sites for breeding will be the most successful conservation measure for A. noctua.

A. noctua colonized central Europe during the beginning of traditional farming practices in this region.  A. noctua is a Eurasian- and Mediterranean steppe species.  There is the question of whether species whose biogeographical core-distribution is located outside of central Europe should be target-species for nature conservation in central-European countries.  More than 70% (136 species) listed in the European Birds Directive have their core distribution outside of Europe.  Nevertheless, this secures investment in the designation of protected areas for these species.  However, it may be of higher conservation value for these countries to focus on species whose core distribution is in central Europe.

LINK to Habel et al.'s 2015 article in Biodiversity and Conservation.

Butterfly diversity in Prague

Intense increases in urbanization worldwide are causing ecologists and conservation biologists to increase their focus on urban areas.  Responses of butterflies to urbanization have been studied in various regions of the world, and studies agree that densities of specialized species decrease towards city centers.  Species that exploit urban environments have been observed to reach higher densities in cities than elsewhere; and in the case of butterflies, these species may depend on ornamental plants.  Population densities of species that are suburban-adaptable are lower in cities than in rural landscapes, and there should be conservation efforts focusing on enhancing populations of suburban-adaptable species and species that tend to completely avoid urban environments, as populations of these species are more likely to be threatened and declining.

To efficiently conserve butterfly populations, knowledge of the distribution of individual species is required, as well as an understanding of how species respond to urbanization.  Local studies from individual cities may show us general patterns that may be applicable between different geographic regions.  Researchers in Prague, Czech Republic, addressed this by comparing local butterfly communities (including burnet moths) observed in 25 urban reserves and parks.

With 88 nature reserves (total area of 2350 hectares), Prague harbors a noteworthy diversity of species.  This is due to Prague's rugged terrain, diverse bedrock, and its location in a warm Vlatava River valley.  These nature reserves consist of a broad diversity of habitats including wetlands, old-growth forest, and dry grasslands on rocky slopes.  Towards the city center, nature reserves are replaced by parks.

85 butterfly species (47% of total butterfly species in Czech Republic) were recorded in the Prague butterfly study, and 22 of the species recorded are threatened in Czech Republic.  The three most species-rich sites (Prokopske udoli, Dalejsky profil, Radotinske udoli) were associated with deep calcareous valleys with rich- and diverse ecosystems, from rocks to grasslands and woodland.  The most species-poor sites were parks near the city center, or small nature reserves with high proportions of forest cover.

Butterfly communities inhabiting Prague's nature reserves and parks were shown to respond positively to a gradient from small sites with homogenous conditions (low altitude range, low plant species richness) to large, diverse sites at the outskirts of Prague.  This is in agreement with other butterfly biodiversity studies.  Sites with suitable conditions for diverse butterfly assemblages are typically far from the city center, as there is more unaltered space in the city's peripheral areas.  Therefore, as in other butterfly studies in urban areas, it was observed that butterfly communities change along a gradient of urbanization.  Habitat availability is the most likely factor shaping a site's butterfly community.  Particularly, sites harboring more plant species will likely contain the larval host-plants of more butterfly species.

From the data in this study, the authors grouped Prague's butterfly species into three categories, regarding each individual species' response to urbanization:  urban-avoiding (increasing outwards from city center), suburban-adaptable (optimum conditions at intermediate urbanization levels), and urban-tolerant (no recognizable response to urbanization).

In Prague, urban-avoiders included some extreme habitat specialists, such as sensitive grassland species (Pseudophilotes vicrama, Pyrgus carthami) and a dry habitat species that requires very large areas of suitable habitat, Hipparchia semele.  Most urban-avoiders were inhabitants of rural woodlands and grasslands; remnants of rural landscape are being increasingly fragmented by urban sprawl, and are practically nonexistent in city centers.

Suburban-adaptable butterflies were the majory of the species observed in this study.  This group contained many dry-habitat species that are supported by large dry grassland reserves in the outskirts of Prague, and also by a dense network of industrial barrens, railways tracks, and abandoned quarries scattered throughout Prague's suburbs.  Some common (Coenonympha pamphilus, Thymelicus lineola) and highly mobile (Issoria lathonia, Inachis io) species were associated with this group, perhaps due to their ability to develop on weedy plants colonizing urban barrens, ot their use of ornamental plants in parks and gardens.  Numerous researchers have indicated that warm- and dry microclimates of industrial- and urban barrens harbor insects.  Approximately one-third of the 85 species (and approximately half of the 60 common species) recorded from this study find their optimum habitat in Prague's suburban belt.  Prague's suburban belt represents an important sanctuary for endangered butterflies.

There were no positive responses to increasing urbanization in this study, indicating that no butterfly species preferred urban environments.  Green areas near the center of Prague provide suitable habitat for arboreal canopy butterflies, but not for grassland butterflies occurring on the ground.  The common grassland butterfly species are absent here most-likely due to inappropriate management of lawns (too frequent- or too clean mowing).  In rural hay meadows, frequent- and uniform mowing has been shown to cause rapid crashes in butterfly populations; and in urban areas this impact on nectar availability for adults, and survival of egg and larva stages, must be even stronger.  Simple, cheap modifications, such as leaving parcels of land unmanaged, would considerably improve to suitability of urban green spaces for butterflies.  Planting selected host plants in parks and gardens would be an additionally-effective measure.  Small measures applied across large urban areas can considerably increase resources for butterflies, increase connectivity between urban nature reserves, and help prevent the loss of species.

LINK to Konvicka and Kadlec's 2011 article in European Journal of Entomology.

Nocturnal moths as pollinators -- and effects of light pollution

Most pollinator studies have focused on insects that are active during daytime, largely ignoring nocturnal insects.  Many nocturnal insects have suffered significant declines.  For example, the populations of two-thirds of the widespread large moth species in Great Britain have significantly declined over the last 40 years.  In addition to bats, beetles, and flies, moths are important nocturnal pollinators; particularly the nectar-feeding species from the moth families Sphingidae, Noctuidae, Geometridae, and Erebidae.  A great diversity of plants, in a wide range of ecosystems, benefit from pollination by moths.

Long-term trends reveal that moth populations have declined, and distributions have narrowed, in Great Britain, the Netherlands, and Finland.  Surely this has been a widespread occurrence elsewhere, though long-term trend data is not necessarily widely-available.  It is likely that habitat degradation and climate change are causing much of these declines, as is the case for diurnal (daytime) pollinators.  Additionally, artificial lighting during nighttime has also been proposed as a cause of nocturnal moth declines.

Moths are well-known to be attracted to artificial lights, often in large numbers.  Shorter wavelengths are generally more attreactive to moths, attractiveness peaking around wavelengths of 400 nm (violet light).  Males of some species have been significantly more-frequently observed at light traps than females, but it is unclear whether this is due to males having a higher attraction to lights, or males being more active and therefore more likely to move into an artificial light's area of influence.  Other than this flight-to-light behavior, moths may be affected by increased ambient light at night, or altered perception of photoperiod in the vicinity of artificial lights.  Additionally, hot components of lamps, or radiant energy from bright lights, can kill insects or damage their wings, legs, and antennae.

Moth reproduction may also be negatively affected by artificial night lighting.  Artificial light can prevent egg-laying, as well as the release of sex pheromones (disrupting mating activity), in some nocturnal moth species.  Artificial lighting could also distract males from female pheromone signals.  In fact, artificial lights have been observed to redirect dispersing- or migrating moths to locations that are unsuitable for breeding, creating an ecological trap for the moths.

Aside from the fact that nocturnal moths are an important food item for numerous other organisms, the loss of these pollinators would certainly lead to the loss of plant diversity, since many plants are reliant on a single- or a few species of moths in order for the plant to sexually reproduce.

LINK to Macgregor et al.'s 2015 article in Ecological Entomology.

Carnivorous pitcher plants as a habitat

In order to obtain nutrients in their nutrient-poor environments, carnivorous pitcher plants trap animals that, once trapped, usually die within a short amount of time.  Animal bodies are dissolved by digestive enzymes produced by the plant, or by mutualistic organisms.  The objective of prey capture is to obtain inorganic nutrients, especially nitrogen and phosphorus.  The epidermis of the trap is composed of a porous cuticle where dissolved nutrients are absorbed.

Carnivorous pitcher plants evolved independently five times in different geographic regions, yet the traps are very similar in all species (Approximately 110 species known).  The uppermost part of the pitcher contains glands that produce nectar and volatiles, which attracts prey.  Prey falls into a hollow leaf, and is unable to climb out due to the ultrastructural composition of the waxy exocuticle (loose wax crystals make climbing impossible for most organisms); the slippery surface at the pitcher margin, and inward-pointing hairs, causes the prey to fall into the pitcher.  The lower part of the pitcher is filled with a fluid that often contains glands for enzyme production.  The biodiversity and ecology of any waterbody is strongly influenced by water chemistry; of all phytotelmata (waterbodies held by living terrestrial plants), carnivorous pitcher plants undoubtedly have the strongest influence over their enclosed waterbody.

In the pitcher plant genera Nepenthes and Cephalotus, closed immature traps already contain fluid which is transferred from the xylem, into the parenchyma, and through glands covering the inner surface of the modified leaf.  Large Nepenthes traps may contain over 1 L of fluid.  The pH of most pitcher fluid is acidic; changes in pH are caused by epidermal cells secreting hydrogen ions.  The fluid of Nepenthes rafflesiana is extremely viscoelatic; the viscoelasticity of the fluid is maintained even after much dilution (up to 95 % dilution), possibly an adaptation to rainfall.  Many pitcher plants have a hood over the trap to keep rainfall from entering the trap.  Surfactants likely occur in several carnivorous pitcher plants, in order to cause drowning of prey by reducing surface tension of the fluid.  Additionally, prey animals stop struggling within a few minutes, which is much faster than in pure water.

Digestive enzymes are found in the fluid of numerous carnivornous pitcher plants; this is an additional energy investment of the plant.  In pitcher plants that do not produce digestive enzymes, a community of organisms within the fluid is essential for breaking down food items.  Some pitcher plants collect non-living organic matter, such as dead leaves.  Aerial (upper) pitchers of a climbing pitcher plant, Nepenthes lowii, lack structures for trapping prey, but still produce nectar.  The nectar of N. lowii is consumed by tree shrews (Tupaia montana) that drop their feces into the pitchers, providing the plant with nutrients.  Still, most carnivorous pitcher plants mainly trap social insects, especially ants.

No species of pitcher plants kills all organisms entering the traps.  Some organisms, from bacteria to amphibians, are able to survive and reproduce within the trap.  For some pitcher inhabitants, pitcher traps are the only habitat in which the species lives.  Pitcher plants grow in different climates, around various plant communities; and different species have differently-shaped pitchers holding fluids with different chemical compositions.  As a consequence of this, they host different inhabitants.  Freshwater animals from most taxonomic phyla inhabit pitcher plants.  Flies are the most diverse animal order found in pitchers; their mobility, along with their well-developed eyes and sense of smell, allows them to find the pitchers in which they lay their eggs.  Misumenops thienemanni and other crab spiders (family Thomisidae) enter pitcher fluid while hanging from a strand of silk, overcoming the high viscoelasticity of the fluid by using extremely slow movements.  Other spiders creating a silk net, sealing the pitcher, catching animals that visit the plant.  The frog species Kalophrynus pleurostigma and Microhyla nepenthicola use Nepenthes ampullaria pitchers as nurseries; up to 100 tadpoles of K. pleurostigma can develop within one pitcher.  Up to four trophic levels, including micro-organisms, can be found in a single N. ampullaria pitcher.

Protozoa are diverse and abundant in Sarracenia pitchers.  Most of these protozoa tolerate low water quality, which is expected due to the presence of dead prey.  Bacterial diversity is unknown; most grow on decaying prey.  Diversity and abundance of fungal hyphae in pitchers are low.  Approximately 70 % of all Sarracenia pitchers are inhabited by the rotifer Habrotrocha rosa, while other rotifers are rare.  Colonization of rotifers occurs by individuals attaching themselves to female pitcher-plant mosquitoes (Wyeomyia smithii).  As in Nepenthes pitchers, arthropods are the most diverse group inhabiting Sarracenia pitchers; this includes crustaceans, mites, spiders, and insects.  The food-webs in Sarracenia traps are quite similar to the food-webs in Nepenthes traps.  As Sarracenia fluid lacks digestive enzymes, micro-organisms most likely play a large role in prey degradation.

Pitcher plants of the genus Heliamphora are restricted to relatively-inaccessible table mountains, and few observations are documented.  Although the bacteria communities in Heliamphora are similar to those found in Sarracenia purpurea, fungi are more abundant in Heliamphora.  Regarding insects, only two species of pitcher-plant mosquitoes are regularly found in Heliamphora.  As with Nepenthes and Sarracenia, spiders create silk webs at the opening of Heliamphora pitchers.

Little is known about the inhabitants of the pitcher-traps of carnivorous bromeliads.  Notably, the bladderwort Utricularia humboldti was reported to colonize these traps; U. homboldti is the only vascular plant known to inhabit pitcher-traps.

In order for a species to establish a population within a pitcher trap, the species must first occur in the same habitat as the pitcher plant.  Then the organisms have to find a pitcher.  Micro-organisms enter traps by rainfall washing cells and spores from the air into the traps, or they may be attached to other organisms entering the pitcher fluid.  Pregnant female pitcher-plant mosquitoes actively search for traps as habitat for their larvae, showing a preferrence for unoccupied traps.  Next, survival in the pitcher fluid must be possible for a population of inhabitants to persist there; most organisms are unable to survive in the fluid.  Finally, resources must also be available for the inhabitants.  In pitchers of Sarracenia and Nepenthes, protists and bacteria are more abundant when the fluid contains more organic nutrients.  In pitchers of Sarracenia purpurea, populations of crab spiders and pitcher-plant mosquitoes are limited by the availability of drowned prey.  In contrast, amphibian tadpoles obtain nutrients from their own yolk until metamorphosis.  Research indicates that a higher species diversity of pitcher-fluid inhabitants increases the stability of pitcher-fluid communities.  Long-term survival is also determined by the life-span of the pitcher, and by the drying- or freezing of the pitcher-fluid.

Some pitcher-trap inhabitants may damage the pitcher or extract nutrients, thereby acting as parasites and parasitoids.  Algae are often abundant in pitcher fluid, consuming dissolved inorganic nutrients.  Caterpillars inhabit pitchers of Nepenthes and Sarracenia, feeding on the inner wall, which leads to the loss of the plant's trapping ability and destruction of the pitcher.  The weevil Metamasius callizona feeds on the meristem tissue at the bottom of C berteroniana pitchers, killing the plant.  The presence of tadpoles in Nepenthes ampullaria pitchers is most likely a commensal relationship, but the mating parents damage the pitchers.  A pitcher's trapping success is reduced by visitors feeding on the plant's prey; these parasitic visitors include crab spiders, the ant Camponotus schmitzi, apes, geckoes, crabs, mantises, among other animals.  Interestingly though, in Sarracenia and Nepenthes pitchers, visitors catch caterpillars that eat the pitchers.

Other pitcher-trap inhabitants may help the plant digest prey.  In pitcher plant species without digestive enzyme production, pitcher inhabitants degrade- and oxidize prey-derived macromolecules, improving a plant's ability to consume these nutrients.  Nepenthes species with poor digestive enzyme production allow bacterial growth by avoiding extreme pH of the pitcher fluid.  Within pitcher fluid, nutrients absorbed by bacteria are partly recycled back to the plant by animals feeding on the bacteria; an average Sarracenia purpurea pitcher hosts 388 ± 924 (range 0 - 960) rotifers (Habrotrocha rosa) feeding mainly on bacteria.  Phosphorus is excreted as phosphate, and 70 % of nitrogen excreted is in the form of ammonium.  Fly larvae also feed on the plant's prey and excrete nitogen in the form of ammonium.  Large insect larvae perform the additional task of physically breaking up prey items, improving accessibility for digestive enzymes and smaller organisms.  However, when insects leave the pitchers, they take valuable nitrogen and phosphorus with them.

Certainly carnivorous pitcher plants have some influence over the communities inhabiting the pitcher fluid.  There is growing evidence for the presence of toxic substances, digestive enzymes, radicals, detergents, narcotics, gelling agents, and acids in the fluid of some pitcher plant species.  The fluid is supplied with oxygen through gaps in the cuticle of the pitcher's inner walls.  Carbon dioxide produced by the fluid's inhabitants is easily absorbed by the leaf (pitcher), while photosynthetic oxygen easily diffuses into the fluid to be used by the inhabitants.

LINK to Adlassnig et al.'s 2011 article in Annals of Botany.

Bees in Europe -- and pollinator research in Greece

There are 1,965 bee species in Europe (~20,000 species on Earth).  Bee species diversity in Europe is partially due to its Mediterranean areas which provide excellent conditions for many bees, and mapping of bee diversity in Europe (figure 1) shows a general increase towards the Mediterranean areas.  ~400 of Europe's bee species are endemic to Europe.  Many of these are associated with mountains and other high elevation habitats, the Canary Islands, Mediterranean islands, and the Mediterranean peninsulas of Spain, Italy, and Greece.

While collecting pollen and nectar, pollen attaches to the insect's body.  The result is that bees transfer pollen grains from flower to flower.  In this way, they help plants sexually reproduce.  Some plants can only be pollinated by certain species.  Therefore, the loss of bee diversity can lead to loss of plant diversity.  A recent European regional assessment has reported the status of all 1,965 European bee species.  The geographic range of this assessment extends from Iceland in the west to the Ural Mountains in the east, and from Franz Josef Land in the north to the Mediterranean in the south.  The Canary Islands, Madeira, and the Azores were also included.

9.2% of bee species are considered threatened at the European level, though this proportion is uncertain due to the high number of species for which there is insufficient data.  For 56.7% of the bee species in Europe, there was not enough data to evaluate the risk of extinction; these species were classified as data-deficient.  The honey bee (Apis mellifera) has been evaluated as data-deficient on the European Red List.  This species is native throughout Europe (except Iceland, the Faeroe Islands, northern Scandinavia, and the Azores), but it is not known whether the species still has self-sustaining wild populations in Europe.

Compared to all other European wild bees, bumblebees are the best-studied group.  According to the European Red List, 23.6% of bumblebee species are threatened with extinction, and populations are decreasing for 45.6% of bumblebee species.  Land-use changes resulting in loss of natural environment is a serious threat to many bumblebees in Europe.  The amount of habitat for the critically endangered bee species Bombus cullumanus has been greatly diminished, resulting in an 80% population loss, in the last decade.  A primary cause of this has been farming practices that involve removing clovers, the main food source for B. cullumanus.  This bee species was previously widespread, but now only exists in a few locations across Europe.  Additionally, Bombus fragrans (the largest bumblebee species in Europe, and red-listed as endangered) is also seriously threatened by intense agricultural land-use, as this is destroying areas of its native habitat in the steppes of Ukraine and Russia.  Rising temperatures and extended periods of drought are also responsible for major changes in bumblebee habitat.  For example, Bombus hyperboreus (the second largest bumblebee species in Europe, and red-listed as vulnerable) is strictly limited to Scandinavian tundra and the extreme north of Russia.  Continued climate change is likely to dramatically reduce B. hyperboreus's habitat and lead to population losses.

The geographic distribution of bee species richness in Europe is shown in figure 1.  The relatively low bee diversity observed on the Balkan Peninsula, north of Greece, is most likely the result of the relatively low amount of research and sampling effort conducted in this region.

Figure 1:  Geographical distribution of bee species richness in Europe.


The geographic distribution of bee species endemism in Europe is shown in figure 2.  There is a high number of endemic bee species in southern Europe.  Similar to the species richness map, the relatively low bee endemism observed in large areas of the Balkan Peninsula is most likely the result of the relatively low amount of research and sampling effort conducted in this region.  Many southern-European bee species also occur in neighboring areas of Asia and north Africa.  Though these species are endemic to these biogeographic regions, they are not represented in figure 2.

Figure 2:  Geographical distribution of bee species endemism in Europe.


The expansion- and intensification of agriculture is a major threat to bees in Europe.  Associated with this is the loss of natural habitat, widespread use of insecticides and herbicides, and livestock farming (resulting in grazing regimes that are damaging to grasslands and fragile ecosystems).  Additionally, the increased frequency of fire in Mediterranean ecosystems, immediately followed by grazing on these post-fire plant communities, decreases bee diversity in these fragile ecosystems.

Urban- and commercial development is another major threat to bees in Europe.  Tourism in coastal regions has led to increases in local populations and number of hotels.  It is estimated that by 2020 there will be ~350 million tourists visiting the Mediterranean coastal region.  Along the mainland Mediterranean coasts of Spain, France, and Italy, 75-80% of the coastal sand dunes have been destroyed by tourism, urbanization, and industry.  Sand dune ecosystems in Greece and Portugal are also under urbanization pressure.  These threatened ecosystems are home to bee species such as Osmia balearica and Osmia uncicornis.  In alpine regions of Europe, a large amount of natural habitat has been converted to ski areas or has been destroyed for other tourism-related infrastructure development.  Red-listed alpine bees such as Bombus brodmannicus are threatened by skiing-related development.  An additional threat related to urban development, sea walls in low-lying coastal areas heavily impact coastal habitats, especially saltmarshes.  This directly impacts specialized endemic bee species such as Colletes halophilus.

Numerous projects, both restoration practice- and scientific research-based, currently address various threats to pollinators, though our knowledge on pollinator diversity, population dynamics, and threats remains limited.  And as mentioned above, there is insufficient data for many, if not most, pollinator species and populations.  The POL-AEGIS project represents a pioneer effort to fill gaps of knowledge.  This project focuses on a wide range of the Aegean archipelago, and the project spans from january 2012 to september 2015.  The aims of the project are to assess pollinator diversity (ecological and genetic) and investigate the causes of pollinator diversity loss.  Here, bees are not the only pollinators studied, and this allows for a more holistic approach to understanding the status of the region's pollinator communities.  Successful achievement of the aims of this project are expected to increase pollination studies and help in creating a regional Red List of pollinators.  Diversity assessments are conducted on 8 islands of the Aegean archipelago (figure 3), individually selected to collectively cover a wide geographical- and climatic gradient within the Aegean Sea and the Sea of Crete.

Figure 3:  Overview of the project's fieldwork areas shown for different work topics.


Of all 33 European countries, Greece has the highest density of honey bee hives, and beekeeping in Greece is increasing.  So far no study has addressed the question of whether solitary bee diversity is affected by competition from honey bees.  Part of the POL-AEGIS project is to examine the effect of hive density on the foraging efficiency, reproduction, diversity, and pollination effectiveness of wild bees.  The project also examines how plant-pollinator networks are infuenced by various grazing intensities, and this will result in valuable knowledge regarding pollinator conservation in Mediterranean regions with livestock, as well as allow for pasture management recommendations.  A third aim within the POL-AEGIS project is to examine the impacts of fire on pollinator diversity, pollination services, and plant-pollinator networks.  This part of the research will be conducted in areas that were heavily burnt within the last few years in Greece.  The results are expected to provide new knowledge for making post-fire management recommendations.

The POL-AEGIS project will communicate its results in scientific articles, books, conference presentations, websites, and Greek popular science journals (e.g. Melissokomiki Epitheorisi -- Apicultural Review), and the project uses a scientific approach alongside community outreach.  Researchers have the large task of systematic collection of pollinators throughout a very fragmented region, and this is taking place at an unprecedented scale.  The results will be valuable for society at several levels.  Locally, bee-friendly management will allow farmers to improve crop quality, help beekeepers to practice balanced apiculture, and provide a more holistic view of nature for wildlife conservationists and land managers.  Regionally, the results of the POL-AEGIS project will provide baseline data useful for future monitoring and sustainable pollinator conservation.

LINK to Nieto et al.'s 2014 article, prepared by IUCN (International Union for Conservation of Nature), and published by the European Commission.
LINK to Petanidou et al.'s 2013 article in Journal of Apicultural Research.

Giant clams -- and restoration in the Philippines

Giant clams are the largest bivalve molluscs, and they live in the warm seas of the Indo-Pacific region.  There are ten known species of giant clam.  The dorsal body wall, or mantle, of all giant clam species is a habitat for a symbiotic photosynthetic algae (Gymnodinium microadriaticum), and during the day, a giant clam opens its shell and extends its mantle tissues so the symbiotic algae can receive sunlight needed for photosynthesis.  Therefore, giant clams are only found in relatively shallow and clear waters, including those associated with coral reefs; the deepest known giant clam occurrence is 20 meters.  Giant clams are filter feeders on particulate organic matter, and the metabolic products of their symbiotic algae provide them with an additional source of nutrition.

Depending on the species, a giant clam reaches maturity after 4 to 9 years.  They reproduce sexually and produce both eggs and sperm, and they cannot self-fertilize.  Through chemical signalling, many individuals synchronize the release of sperm and eggs into the water (broadcast spawning), and this helps ensure fertilization.  Spawning seems to occur during incoming tides; spawning is intense for 30 minutes to two-and-a-half hours, with contractions occurring every 2 to 3 minutes.

A fertilized eggs floats in the sea for about 12 hours until hatching into a planktonic larva.  It then begins to produce a calcium carbonate shell, and soon develops a "foot" which is used to move on the substrate.  Larvae can also swim to find suitable habitat.  Giant clam larvae do not host symbiotic algae, and rely completely on filter feeding.  After about one week, the giant clam settles on the substrate, though frequently changing locations during the first weeks.  The largest giant clam, Tridacna gigas, can grow to weigh over 200 kg, measure 120 cm in length, and has an average lifespan in the wild of 100 years or more.

The distribution of giant clams (figure 1) spans from south- and east Africa to the east Pacific beyond French Polynesia (between 30°E and 120°W), and from Japan to Australia (between 36°N and 30°S).  Tridacna maxima has the widest distribution, and the greatest species diversity of giant clams is observed in the central Indo-Pacific.  Seven species can be found in southeast Asia, but many populations are declining dramatically, and there are cases of local extinctions.  Local extinctions of giant clam species have been reported in areas of the Philippines, Indonesia, Micronesia, Malaysia, and Singapore.  Giant clams can be found throughout Oceania (Australasia, Melanasia, Micronesia, and Polynesia).  While abundance of giant clams in Oceania has been declining, there are areas in Oceania with unusually high abundances, including the Ashmore, Cartier, and Mermaid reefs of Australia.

Figure 1:  Distribution of giant clams.  Blue triangles represent non-scientist observations where species is unknown.


Their numbers have been greatly reduced due to overharvesting and loss of habitat, and giant clams are also seriously affected by increasing sedimentation and pollution.  Furthermore, increasing sea surface temperatures leads to the loss of symbiotic algae.  Eight species of giant clam are red listed as conservation-dependent or vulnerable; another species, Tridacna costata, was only recently discovered and is therefore not yet listed, though "critically endangered" is the proposed appropriate category.

A number of countries including Tonga, Palau, Fiji, Soloman Islands, and Cook Islands, have attempted to restore giant clam populations through local aquaculture- and restocking programs.  The Marine Science Institute (MSI) at the University of the Philippines has a long and successful record of rearing cultured giant clams to restore populations.  The restocking of giant clams in the Philippines began in 1987 as interest grew among private and public sectors for establishing giant clam ocean nurseries.  A collaborative research program for culturing bivalves was organized, the MSI being one of the participants in the program.  Key objectives of the restocking program were to establish broodstocks and develop culturing techniques, with the aims of mass-production for restocking and creating livelihoods around giant clam farming.

Field surveys around the Philippines indicated that the 3 largest giant clam species were rare.  In fact, only 2 wild sub-adult Tridacna gigas, and no Hippopus porcellanus, were found.  Restocking started slowly, as only a limited number of giant clams were available to place in the wild, and restored populations initially suffered heavy losses due to poaching and illegal fishing.  Eventually, individuals and groups teamed up to protect giant clams, and marine protected areas became regarded as suitable sites for restocking giant clams.

Scuba divers collected gametes (sperm and eggs) in plastic bags and took them to the boat where gametes of different individuals were mixed, thereby fertilizing the eggs.  Hatchery-raised giant clams were released as juveniles throughout the Philippines, and stewards were trained to monitor the survival and growth of restocked clams.  Giant clams have been restocked at more than 40 sites (figure 2) spread over more than 20 coastal provinces of the Philippines.  The northern region (Luzon) has received the greatest number, as it is close to MSIs hatchery.  The Hundred Islands National Park in the north has been another region of focus due to a special project funded by the Philippine Tourism Authority.

This giant clam restoration initiative has increased collaborator interest in protecting- and culturing giant clams, and improvements in practices and methods have provided valuable lessons to the restoration practitioners involved.  One important lesson learned is that restoring giant clam populations must include the strong commitment of local communities.

LINK to Othman et al.'s 2010 article in The Raffles Bulletin of Zoology.
LINK to Gomez and Mingoa-Licuanan's 2006 article in Fisheries Research.

Indo-Malayan peat swamp forests

The peat swamp forests of the Indo-Malayan region are generally recent formations (<5000 years old) over oceanic muds and sands in coastal lowlands.  These are unusual ecosystems.  Despite extreme conditions (pH of 2.9 to 4; nutirent-poor; anaerobic; unstable peat substrate 20 m deep or more; forest floor flooded during wet season, and waterlogged during dry season), trees in these swamps can grow over 70 m tall.  Rainfall and oceanic aerosols are the sole water inputs; there are no river inflows to make these ecosystems nutrient-rich.

927 species of flowering plants and ferns were recorded in the peat swamps of Borneo.  In peninsular Malaysia, 260 species of plants were recorded.  Bladderworts (Utricularia spp) are observed ingesting very small animals and protozoans, mostly for obtaining nitrogen and phosphorus in these nutrient-poor environments.  Other plant adaptations in these forests include buttress roots and stilt roots which provide stability in the peat, and respiratory roots which grow from the stem or up from burried waterlogged roots.

Malaysian peat swamps have a rich biodiversity of aquatic invertebrates, though lacking molluscs, leeches, and organisms that require rocky substrates and flowing waters. There are many undescribed aquatic invertebrate species.  Vertebrates are generally more well known in these ecosystems.  Over 200 species of fish have been recorded in the peat swamps of peninsular Malaysia, Borneo, and Sumatra, including the world's smallest known fish (Paedocypris progenetica) (7.9 to 10.3 mm long at maturity) which was recently discovered in the peat swamp forests of Sumatra.

Elephants, tapirs, leopards, tigers, rhinoceros, orangutans, and proboscis monkeys all live in peat swamp forests.  57 mammal species (excluding rodents and bats) and 237 bird species have been identified in Malaysian peat swamp forests.  Of these species, 51% of the mammals and 27% of the birds are on the IUCN Red List of Threatened Species.  As with the aquatic invertebrate communities, the amphibian and reptile communities of peat swamp forests are not well known.  The most threatened organisms in these ecosystems are those that are specialized in inhabiting peat swamp forest, as generalist species are surviving in areas that are being degraded.  The loss of habitat specialists is likely to have severe negative impacts on ecosystem function.  

With the present push from Europe for palm oil production, the conversion of peat swamp forests to oil palm plantations is increasing.  Additionally, the water from peat swamps is used to irrigate oil palm- and rice plantations.  It is important to note that the conversion of these peatlands to oil palm plantations has no merit, as the destruction of peat swamp forest results in carbon dioxide emissions that are up to 36 times greater than the amount saved by the European countries' switch to using palm oil biodiesel.

There are efforts to restore degraded peat swamp forests in Central Kalimantan.  The target is to restore and conserve 80% of the former Mega Rice Project area.  This effort involves restoring swamp hydrology through dam construction and blocking canals that were built to drain peatlands.  Indigenous inhabitants have constructed a variety of dams, and canals are becoming filled in naturally by leaf litter and other plant debris.  These dams are constructed of timber (sometimes with added sandbags for support) and become increasingly permanent as they trap plant debris and become vegetated.  Additionally, restoration measures include replanting indigenous plant species that will help rebuild the peat layers, and various mounting systems are being used to keep seedlings from being submerged.  Currently it appears that rehabilitation will be successful in mildly degraded areas.

LINK to Catherine Yule's 2010 article in Biodiversity and Conservation.

LINK to the Katingan Project's website.