Biodiversity and global change
Created | Updated Jan 28, 2002
Loss of biodiversity in a changing global environment
1/ Introduction
Environmental change will affect biodiversity in a number of ways, including shifts in distributions of plants and animals, barriers to species migration, and changing patterns of precipitation and evaporation. The key variable is time: rates of change will be variable, but in many cases species will be unable to react quickly enough to changes in climate or habitat fragmentation.
2/ What is biodiversity?
Biodiversity is popularly defined as species richness, or the number of species in an area (Chapman & Roberts 1997). Studies of food webs show that the average number of species with which any one species interacts is consistently between 3 and 5. In stable environments, the number is consistently higher (average 4.6) than in fluctuating ones (average 3.5) (May 1988).
Ecosystem diversity may be a more meaningful way of defining and evaluating biodiversity. Variety within and between ecosystems provides more niches for species to thrive in (Morell 1999). Roy & Tomar (2000) suggest a policy shift has occurred in conservation, from identification of single species to an understanding of habitat functions. Researchers consistently report that habitat destruction reduces the ability of ecosystems to withstand disturbance and contributes to species decline (Nystrom et al 2000, Corser 2001).
Van Straalen (1999) suggests that genetic variation within species has received less attention than species richness and ecosystem diversity. Yet this threat to biodiversity is perhaps the most insidious threat to human survival (Ayres 2000). Genetic variation enables species to withstand pathogen attack and other disturbances. Habitat loss causes populations to crash, thus reducing the gene pool due to inbreeding and rendering species more vulnerable to pathogens; in addition, crowding due to habitat loss has placed species closer than in natural conditions, enabling pathogens to jump species.
A number of research papers focus on the concept of functional diversity. White et al (2000) found that functional diversity is a greater determinant of ecosystem productivity than species richness, because functions are species-specific. Therefore, species with similar functional attributes compensate for those species removed by a disturbance. Similarly, Duarte (2000) established that ecosystem functions are dependent upon the particular membership of the community, rather than number of species. Both papers acknowledge that increasing species richness strengthens the functional repertoire of a community (Duarte 2000, White et al 2000), thus the link between biodiversity and ecosystem function is indirect, but crucial.
The insurance hypothesis states that species richness increases community-level stability by ensuring that some species in a community are tolerant of environmental fluctuations (Ives et al 2000).
3/ Why do some areas contain greater diversity than others?
We do not fully understand the processes of biodiversity (Bengtsson et al 2000), but a number of hypotheses suggest reasons for the geographical distribution of diversity:
Time ; areas of high biodiversity experienced less environmental upheaval throughout geologic time, thus enabling speciation to continue uninterrupted
Stability ; areas with stable conditions contain higher diversity. Thus, species richness is strictly connected with climatic factors: the amount of environmentally available energy limits distribution. Species richness is found to increase from tundra to forest. (Shvarts et al 1995)
Refugium ; forests retreated during the last glaciation to form islands of biodiversity, which encouraged allopatric speciation. Thus, refugia of south, south-west, and south-east Europe contain greater diversity than the rest of the continent (Bengtsson et al 2000).
Niche ; tropical forests contain more niches for species to specialise in. Therefore, high rates of endemism are common within the forests. Some species of beetle may only exist on individual trees (Morell 1999).
Although our knowledge of the processes of biodiversity is sketchy, we have a better idea what causes the loss of biodiversity.
4/ Extinctions and loss of biodiversity
It is the fate of all species to go extinct. The fossil record indicates that most species exist for around 4 million years; thus, 25% of species have a good chance of becoming extinct every million years (Chapman & Roberts 1997). The background extinction rate is between 1 and 7 species per year (Jeffries 1997), yet there have been 5 mass extinction events and eleven further major declines in the last 6 million years (Harrison 1997). The extinction rate during these mass holocausts may be between 15 and 30 species per year, yet some estimates put current extinction rates at 4000 species per year (Chapman & Roberts 1997, Jeffries 1997). We are living in, and fuelling, the sixth extinction event: some 50% of species could be annihilated in the 21st century (Morell 1999).
The cause of mass extinctions is the subject of much debate. Some researchers believe a meteorite impact caused the Cretaceous extinction, yet Hallam & Wignall (1999) suggest all five events were prompted by eustatic sea-level rise. Other possible causes are global cooling, volcanic eruptions, or the Pangaean super-continent exposing species to over-intense competition (Harrison 1997).
EVENT
Ordovician
Devonian
Permian
WHEN?
Triassic
Cretaceous
440 million years ago
370 million years ago
250 million years ago
CONSEQUENCES
210 million years ago
65 million years ago
25% of families lost
19% of families lost
54% of families lost; the most catastrophic loss of life thus far; extinction of trilobites; perhaps 90% of all pre-existing species wiped out
23% of families lost
17% of families lost; dinosaurs extinct; up to 75% of species killed off
Table 1: The 5 mass extinction events, from information in Harrison (1997) and Morell (1999).
In Hallam & Wignall (1999), species decline is theorised to have started by sea-level change causing extinction on the continental shelf; yet the authors accept that, in the case of the Cretaceous event, meteorite impact may have delivered the final coup de grâce. This is an important concept, and one which runs consistently throughout the literature: species decline is almost certainly not caused by single processes, but rather by a chain of disturbances which ecosystems cannot withstand. For instance, the population collapse of amphibians since the 1970s is ultimately blamed on habitat loss, but other factors (over-collecting, increased UV-B radiation, pathogen epidemics, etc) act in concert to precipitate the decline (Corser 2001).
No two species can live side by side from exactly the same resource: thus, species diversify to exploit different niches and microhabitats. Yet humans exploit every niche (Harrison 1997): human activities (habitat destruction, pollution, hunting, collection, etc) represent a relentless assault on natural ecosystems, from which there is no time to recover.
The current ecological conceptual framework is that ecosystems are dynamic systems in which change and disturbance are natural (Bengtsson et al 2000, Dale et al 2000). When disturbance exceeds its natural range of variation, however, the consequences are extreme. Humans alter the natural disturbance regimes of ecosystems and make it impossible for recovery to take place.
Table 2: natural disturbance regimes of corals (Nystrom et al 2000)
Process
Predation & grazing
Coral collapse
Bleaching
Storms
Hurricanes
Mass bleaching
Crown-of-thorns
Epidemics
Sea-level or temperature change
Spatial extent
1 -10 cm
1 m
1 m
1 -100 km
10 -1000 km
10 -1000 km
10 -1000 km
10 -1000 km
Global
Frequency
Weeks -months
Months -years
Months -years
Weeks -years
Months-decades
Years -decades
Years -decades
Months-century
Millennia
Duration
Minutes -days
Days -weeks
Days -weeks
Days
Days
Weeks -months
Months -years
Years
Millennia
In a study of coral reef resilience, Nystrom et al (2000) suggest that human activities alter the natural disturbance regimes of corals by transforming pulse events into persistent and chronic stress. Pulse disturbances include over-grazing by algae, peaks of predator populations, hurricanes, sea-surface temperature change, and so on. These events cause renewal and development in corals, yet with human pressure added in, the corals do not have time to recover. This pressure may be direct (dynamite fishing, collection by tourists, or removal for construction material) or indirect, as corals are passive receivers of the impacts of global warming, sedimentation caused by deforestation, eutrophication, and pollution (Nystrom et al 2000, Reaser et al 2000).
Biodiversity is threatened by four interacting mega-phenomena (Ayres 2000):
Human population growth
Energy and materials consumption
CO2 concentrations
Species extinctions
There is much in the literature which supports the suggestion of Ayres (2000) that mutually interacting phenomena cause environmental crises. When analysing species extinction and loss of biodiversity, therefore, we should not try and identify single causes.
5/ Trends in current research
Our knowledge of species richness is poor; of an estimated total of 30 million species, less than 2 million have been identified (Jeffries 1997). Furthermore, our knowledge of the processes of biodiversity is in its infancy (Bengtsson 2000). Research in the field is focused upon trying to understand how ecosystems will respond to environmental change, and what the impacts of species extinctions will be upon ecosystem function. Concern is raised at the rate of species decline, occurring faster than at any time in the past (Morell 1999). As May (1988) states:
"Conservation biology is a science with a time limit, with the clock ticking faster as human population increases."
5a/ Modelling in biodiversity research
Zacharias et al (2000) proposed a hierarchical approach to conserving marine biodiversity, by conceptualising structural and functional attributes at genetic, population, community, and ecosystem levels within ecological models. The authors contend that this type of framework is good for understanding the relationships between structure and process, and how those relationships change between levels. Thus, efforts to protect single species are misguided, because that approach ignores the interactions between a species and its environment (Zacharias et al 2000).
Price et al (1999) looked at the suitability of gap-phase dynamics,or patch models, for simulating the sensitivity of boreal ecosystems to climate variability. The authors identified a problem in that models use mean climate values, when in reality species presence/absence may be due to infrequent extreme climate anomalies, such as killing frost. Arguing that extreme events will increase in frequency with global warming, Price et al (2000) conclude that modelled predictions should be treated with caution; we need to find a way of incorporating climate variability within models.
Mapping patterns of biodiversity using Geographical Information Systems (GIS) and remote sensing is attempted by Roy & Tomar (2000). This type of geospatial modelling will, the authors contend, help in conservation by making continuous monitoring easier, and by providing systematic inventories of ecosystem diversity.
Cumming (2000) attempts to map biodiversity by using regression models to produce a probability surface of species distribution. Using existing data on distributions, the author modelled where it was probable that a certain species exists and concludes this approach is better than attempting logistically arduous presence/absence maps.
Shvarts et al (1995) attempt to predict future patterns of biodiversity by projecting present correlations in spatial variability in climate and biodiversity into the future. The authors conclude that species richness is strictly connected with climatic factors, with continentality and aridity the primary factors. Similarly, Smith et al (1995) model future distributions of latitudinal vegetation belts by comparing the climate simulations of four General Circulation Models (GCMs) at double present CO2 concentrations (see Table 3).
Current OSU GFDL GISS UKMO
TUNDRA 939 -302 -515 -314 -573
DESERT 3699 -619 -630 -962 -980
GRASSL 1923 380 969 694 810
DRY FOR 1816 4 608 487 1296
MESIC 5172 561 -402 120 -519
Table 3: changes in areal extent of vegetation zones (km² x 10 000). From Smith et al (1995). (OSU = Oregon State University; GFDL = Geophysical Fluid Dynamics Laboratory; GISS = Goddard Institute for Space Studies; UKMO = United Kingdom Meteorological Office)
Despite a discrepancy between wet and dry forests (GFDL and UKMO predicted losses of mesic forests, but larger increases in dry forests), the total area of forest is predicted to increase (Smith et al 1995). Since tropical forests contain the greatest biodiversity, an increase in their extent should result in an increase in species diversity; yet GCMs only predict climate conditions which could favour particular vegetation.
Duckworth et al (2000) used a model to predict the effect of climate change on European grasslands, and found that the potential for change is reduced when environmental factors other than climate are included (eg: soil type), and when vegetation is considered as a whole rather than on an individual species basis. Interactions between climate and other factors need to be incorporated into models of future biodiversity patterns.
Climate is a major control on vegetation distribution, yet other factors act in concert to influence the process. Unless an 8000-year trend is reversed, we may expect land clearance for agriculture to diminish the areal extent of forests.
5b/ Response to greenhouse-induced climate change
Dale et al (2000) look at the interplay between climate change and forest disturbance. Disturbance is seen as a natural and integral component of forest ecosystems, to which climate change is an added stress. The authors conclude that future projections of biodiversity in forests must take into account how climate controls the frequency, intensity and type of disturbance.
Similarly, Ayres & Lombardero (2000) consider the impacts of global change on pathogen and herbivore disturbance in forests, stating that even modest climate change will have large impacts because insects and pathogens have short life cycles, have high reproductive potential, and are mobile. The authors call for further research into the effect of climate variability and climatic extremes on the distribution of pathogens, and the incorporation of feedbacks into future models.
Reaser et al (2000) found that coral bleaching in 1998 was almost certainly due to global warming, as tropical sea-surface temperatures were the highest on record. Furthermore, bleaching was world-wide and thus not attributable to local stresses. Corals are good ecological canaries, because they are vulnerable to high temperatures and are among the first systems to show thermal stress. However, Reaser et al (2000) list other causes of bleaching, including sedimentation and UV-B radiation intensity.
Some papers try to simulate the effects of future climate change on ecosystems. White et al (2000) tested the sensitivity of three grassland communities to enhanced temperature and rainfall. They concluded that species-rich ecosystems were more likely to contain stress tolerant species capable of withstanding disturbance, yet communities with the same species richness performed differently in terms of productivity, due to different functional diversity. C4 plants had greater heat tolerance than C3 plants (White et al 2000).
Grayson (2000) attempted to predict future mammal distributions in the Great Basin of the U.S., by using past climates as analogues. He predicted a loss of mammal species, and an increase in xerophytic plant species, but added the proviso that current warming is due to greenhouse gas forcing, while the analogue climate was warmer due to changing solar radiation. Ungerer et al (1999) found that warming may allow the southern pine beetle to attack forests further north in the U.S., but distribution in the west is limited by lack of host trees.
De Groot et al (1995) suggest criteria for the selection of bio-indicators to assess the possible effects of climate change. Noting that Europe's landscape is already heavily fragmented, the authors suggest climate change is an additional stress which may prove too strong for ecosystems to resist. The authors propose future research is directed at finding suitable species to warn of climate change, and looking at how these climate sensitive species react to changes in temperature and rainfall.
5c/ Response to tropical deforestation and habitat loss
Deforestation is as old as agriculture. Three countries (Brazil, Indonesia, and the Congo Republic) have over 50% of global tropical forest (Harrison 1997). Yet these countries also have enormous populations, and the agricultural frontier continually threatens the forest.
Conversion of variable landscapes to monocultures by humans would almost certainly lead to decline in biodiversity, although at the local scale the relationship is not simple; communal lands in South Africa were found to contain more biodiversity than neighbouring nature reserves (Shackleton 2000).
Biodiversity is ultimately threatened by habitat destruction. Vallan (2000), however, found that amphibians in Madagascar react less sensitively to landscape fragmentation than to climatic change. In this study, the difficulty in establishing a single cause for species decline is illustrated: on further investigation, decline was shown to be due to adverse micro-climatic conditions on the edges of fragments.
Destruction of Australian rainforest has led to the highest global rates of mammal extinctions. Species surviving in the remnant pockets of forest are biologically dead: populations are so small extinction is inevitable within a few decades (Barkham 2000).
Deforestation accelerates the effect of global warming. Grace & Malhi (1999) estimate that a deforestation rate of 0.9% per year is equivalent to an efflux of 1.6-1.9 Gt of carbon. Conversion of tropical forest to farmland contributes 1-2 billion tonnes of carbon to the atmosphere. Lal (1999) analyses the effects of deforestation with regard to carbon sequestration and the greenhouse effect. Robertson et al (2000) state that no cropping systems result in a mitigation of carbon efflux. Thus, natural habitat destruction stresses species by accelerating climatic disturbance.
Duarte (2000) tested the response of a species-poor community to the removal of one species. The response was a decline in productivity in four of the six extant species: partial loss of species diversity leads to further decline in diversity within species-poor communities, confirming the insurance hypothesis that species-rich communities are more likely to withstand disturbance.
5d/ Response to stratospheric ozone depletion
If ozone within the stratosphere continues to be depleted, intense UV-B radiation will affect ecosystems in harmful ways. UV-B radiation causes vegetation to absorb less CO2 via photosynthesis, so more CO2 may accumulate in the atmosphere and cause further global warming (Lichterman 1999).
Studies have shown that enhanced UV-B radiation has a detrimental effect on plant productivity. Li Yuan et al (2000) tested 20 wheat cultivars under simulated conditions equivalent to a 20% depletion of ozone: 19 cultivars showed a negative response, indicating inhibition on growth and crop yield. Under similar conditions, Correia et al (2000) found decreases in yield and biomass production of up to 49% in maize crops.
If natural ecosystems react to enhanced UV-B radiation in the same manner, species richness may decline. We do not know the precise response to UV-B forcing, but perhaps 20% of plants are sensitive (Li Yuan et al 2000). Laakso et al (2001) suggest the effects of UV-B may be cumulative; species response to disturbance will not be abrupt, so the impacts of ozone depletion may not be apparent immediately. For animals, UV-B will cause heat stress, skin cancers, and increasing blindness through cataracts (Lichterman 1999).
5e/ Response to desertification
Investigating the hypothesis that desertification reduces species diversity in mammals, Whitford (1999) found greater mammal diversity in degraded areas than in adjacent desert grasslands. One explanation for this is that grassland species may remain in areas that become degraded, and are joined by species that prefer desertified areas. Vallan (2000) suggests that as habitat dwindles, species richness initially increases due to crowding before declining. Species richness in the areas studied by Whitford (1999) may show a decline in mammal diversity at a later date.
Whitford (1999) concludes that biodiversity is not a good measure of desertification impacts. Since all fauna rely on vegetation for food or shelter, a reduction in soil fertility and consequent decline in vegetation cover can be expected to cause a decline in species richness.
6/ Proposals for future research
The study of environmental change is a new science; there are many feedbacks and interactions between components of the biosphere and atmosphere that we do not understand. Loss of biodiversity may cause great harm to natural and human ecosystems: it is imperative that future research explains the role of biodiversity in ecosystem productivity, and illustrates the danger to humankind of biodiversity depletion.
Usher (2001) calls for more interdisciplinary studies, and many of the articles researched for this report conclude by emphasising the need for refined predictions of future change from allied disciplines. Ayres & Lombardero (2000) list 13 proposals for future research, especially on the interactions and feedbacks between biota and climate. Bengtsson et al (2000) call for more research into the role of biodiversity in ecosystem function and stability, studies of population dynamics, and field tests of the insurance hypothesis. De Groot et al (1995) look for the identification of indicator species which warn of future climate change.
An understanding of the link between biodiversity and ecosystem productivity will show the true value of biodiversity, and refined methods of projecting future patterns of biodiversity may assist in conservation efforts. A shift in emphasis from conservation of single species to protection of ecosystem diversity is a more effective way of protecting biodiversity. We need to move away from disputable aesthetic campaigns for species conservation, and establish the real scientific threat to humankind that the loss of biodiversity represents.
7/ Conclusions
Our knowledge of the processes and value of biodiversity is sketchy, perhaps because it is difficult to observe or measure biotic interactions such as predation and competition. We know more about the causes of species decline, but must not jump to conclusions and blame all ills on individual causes. As the research shows, species response to change is complicated by a number of factors and feedback mechanisms.
It is crucial that we establish the true value of biodiversity to humankind. We need to react now to a changing global environment, and understand the threat posed by the loss of biodiversity. ENDS (3486 words)
References:
Ayres E. (2000) ‘The Four Spikes’ Futures 32, pp 539-554.
Ayres M & Lombardero M. (2000) ‘Assessing the consequences of global change for forest disturbance from herbivores and pathogens’ The Science of the Total Environment 262, pp263-286.
BarkhamP. (2000) ‘Reckless bush clearance may cost Australia the earth’ The Guardian 24/11/2000.
Bengtsson J, Nilsson S, Franc A & Menozzi P. (2000) ‘Biodiversity, disturbances, ecosystem function and management of European forests’ Forest Ecology & Management 132, pp39-50.
Chapman J & Roberts M. (1997)‘Biodiversity: The Abundance Of Life’. Cambridge.
Correia C, Coutinho J, Bjorn L & Torres-Pereira J. (2000) ‘Ultraviolet-B radiation and nitrogen effects on growth and yield of maize under Mediterranean field conditions’ European Journal of Agronomy 12, pp117-125.
Corser J. (2001) ‘Decline of disjunct green salamander (Aneides aeneus) populations in the southern Appalachians’ Biological Conservation 97, pp119-126.
Cumming G. (2000) ‘Using habitat models to map diversity: pan-African species richness of ticks (Acari: Ixodida)’ Journal of Biogeography Vol 27 (2) pp425-440.
Dale V, Joyce L, McNulty S & Neilson R. (2000) ‘The interplay between climate change, forests, and disturbances’ The Science of the Total Environment 262, pp201-204.
De Groot R, Ketner P & Ovaa A. (1995) ‘Selection and use of bio-indicators to assess the possible effects of climate change in Europe’ Journal of Biogeography Vol 22 pp 935-943.
Duarte C. (2000) ‘Marine biodiversity and ecosystem services: an elusive link’ Journal of Experimental Marine Biology and Ecology 250, pp 117-131.
Duckworth J, Bunce R & Malloch A. (2000) ‘Modelling the potential effects of climate change on calcareous grasslands in Atlantic Europe’ Journal of Biogeography Vol 27 (2) pp347-358.
Grace J & Malhi Y. (1999) ‘The role of rainforests in the global carbon cycle’ Progress in Environmental Science Vol 1, No. 2 pp177-193.
Grayson D. (2000) ‘Mammalian responses to Middle Holocene climatic change in the Great Basin of the western United States’ Journal of Biogeography Vol 27, No.1 pp 181-192.
Hallam A & Wignall P. (1999) ‘Mass extinctions and sea-level changes’ Earth-Science Reviews 48, pp217-250.
Harrison P. (1997) ‘The third revolution’. Penguin.
Ives A, Klug J & Gross K. (2000) ‘Stability and species richness in complex communities’ Ecology Letters 3, pp399-411.
Jeffries M. (1997) ‘Biodiversity and Conservation’. Routledge.
Laakso K, Kinnunen H & Huttunen S. (2001) ‘The glutathione status of mature Scots pines during the third season of UV-B radiation exposure’ Environmental Pollution 111, pp349-354.
Lal R (1999) ‘Soil management and restoration for C sequestration to mitigate the accelerated greenhouse effect’ Progress in Environmental Science Vol 1, No.4 pp307-326.
Lichterman J. (1999) ‘Disasters to come’ Futures 31, pp593-607.
Li Yuan, Zu Yanqun, Chen Haiyan, Chen Jianjun & Yang Jilong (2000) ‘Intraspecific responses in crop growth and yield of 20 wheat cultivars to enhanced ultraviolet-B radiation under field conditions’ Field Crops Research 67, pp25-33.
May R. (1988) ‘How many species are there on Earth?’ Science 241 pp 1441-49.
Morell V. (1999) ‘The Sixth Extinction’ National Geographic Vol 195, No.2 pp42-56.
Nystrom M, Folke C & Moberg F. (2000) ‘Coral reef disturbance and resilience in a human-dominated environment’ Tree 15, no 15 October 2000, pp 413-419.
Price D, Halliwell D, Apps M & Peng C. (1999) ‘Adapting a patch model to simulate the sensitivity of Central-Canadian boreal ecosystems to climate variability’ Journal of Biogeography 26 (5) pp1101-1113.
Reaser J, Pomerance R & Thomas P. (2000) ‘Coral bleaching and global climate change: scientific findings and policy recommendations’ Conservation Biology 14 (5) pp1500-1511.
Robertson G, Paul E & Harwood R. (2000) ‘Greenhouse gases in intensive agriculture: contributions of individual gases to the radiative forcing of the atmosphere’ Science 289 pp 1922-25.
Roy P & Tomar S. (2000) ‘Biodiversity characterization at landscape level using geospatial modelling techniques’ Biological Conservation 95, pp95-109.
Shackleton C. (2000) ‘Comparison of plant diversity in protected and communal lands in the Bushbuckridge lowveld savanna, South Africa’ Biological Conservation 94, pp273-285.
Shvarts E, Pushkaryov S, Krever V & Ostrovsky M. (1995) ‘Geography of mammal diversity and searching for ways to predict global changes in biodiversity’ Journal of Biogeography Vol 22, pp907-914.
Smith T, Halpin P, Shugart H & Secrett C. (1995) ‘Global Forests’ in ‘As Climate Changes (Strzepek K & Smith J., eds). Cambridge.
Ungerer M, Ayres M & Lombardero M. (1999) ‘Climate and the northern distribution limits of Dendroctonus frontalis Zimmerman (Coleoptera: Scolytidae)’ Journal of Biogeography 26 (6) pp1133-1145
Usher M. (2001) ‘Landscape sensitivity: from theory to practice’ Catena 42, pp375-383.
Vallan D. (2000) ‘Influence of forest fragmentation on amphibian diversity in the nature reserve of Ambohitantely, highland Madagascar’ Biological Conservation 96, pp31-43.
Van Straalen N. (1999) ‘Developments in genetic biodiversity in toxicant-stressed populations’ Progress in Environmental Science 1 (2) pp195-201.
Whitford W. (1999) ‘Desertification and animal biodiversity in the desert grasslands of North America’ Tektran/US Department of Agriculture
White T, Campbell B, Kemp P & Hunt C. (2000) ‘Sensitivity of three grassland communities to simulated extreme temperature and rainfall events’ Global Change Biology 6, pp671-684.
Zacharias M & Roff J. (2000) ‘A hierarchical ecological approach to conserving marine biodiversity’ Conservation Biology 14 (5) pp1327-1334.
1/ Introduction
Environmental change will affect biodiversity in a number of ways, including shifts in distributions of plants and animals, barriers to species migration, and changing patterns of precipitation and evaporation. The key variable is time: rates of change will be variable, but in many cases species will be unable to react quickly enough to changes in climate or habitat fragmentation.
2/ What is biodiversity?
Biodiversity is popularly defined as species richness, or the number of species in an area (Chapman & Roberts 1997). Studies of food webs show that the average number of species with which any one species interacts is consistently between 3 and 5. In stable environments, the number is consistently higher (average 4.6) than in fluctuating ones (average 3.5) (May 1988).
Ecosystem diversity may be a more meaningful way of defining and evaluating biodiversity. Variety within and between ecosystems provides more niches for species to thrive in (Morell 1999). Roy & Tomar (2000) suggest a policy shift has occurred in conservation, from identification of single species to an understanding of habitat functions. Researchers consistently report that habitat destruction reduces the ability of ecosystems to withstand disturbance and contributes to species decline (Nystrom et al 2000, Corser 2001).
Van Straalen (1999) suggests that genetic variation within species has received less attention than species richness and ecosystem diversity. Yet this threat to biodiversity is perhaps the most insidious threat to human survival (Ayres 2000). Genetic variation enables species to withstand pathogen attack and other disturbances. Habitat loss causes populations to crash, thus reducing the gene pool due to inbreeding and rendering species more vulnerable to pathogens; in addition, crowding due to habitat loss has placed species closer than in natural conditions, enabling pathogens to jump species.
A number of research papers focus on the concept of functional diversity. White et al (2000) found that functional diversity is a greater determinant of ecosystem productivity than species richness, because functions are species-specific. Therefore, species with similar functional attributes compensate for those species removed by a disturbance. Similarly, Duarte (2000) established that ecosystem functions are dependent upon the particular membership of the community, rather than number of species. Both papers acknowledge that increasing species richness strengthens the functional repertoire of a community (Duarte 2000, White et al 2000), thus the link between biodiversity and ecosystem function is indirect, but crucial.
The insurance hypothesis states that species richness increases community-level stability by ensuring that some species in a community are tolerant of environmental fluctuations (Ives et al 2000).
3/ Why do some areas contain greater diversity than others?
We do not fully understand the processes of biodiversity (Bengtsson et al 2000), but a number of hypotheses suggest reasons for the geographical distribution of diversity:
Time ; areas of high biodiversity experienced less environmental upheaval throughout geologic time, thus enabling speciation to continue uninterrupted
Stability ; areas with stable conditions contain higher diversity. Thus, species richness is strictly connected with climatic factors: the amount of environmentally available energy limits distribution. Species richness is found to increase from tundra to forest. (Shvarts et al 1995)
Refugium ; forests retreated during the last glaciation to form islands of biodiversity, which encouraged allopatric speciation. Thus, refugia of south, south-west, and south-east Europe contain greater diversity than the rest of the continent (Bengtsson et al 2000).
Niche ; tropical forests contain more niches for species to specialise in. Therefore, high rates of endemism are common within the forests. Some species of beetle may only exist on individual trees (Morell 1999).
Although our knowledge of the processes of biodiversity is sketchy, we have a better idea what causes the loss of biodiversity.
4/ Extinctions and loss of biodiversity
It is the fate of all species to go extinct. The fossil record indicates that most species exist for around 4 million years; thus, 25% of species have a good chance of becoming extinct every million years (Chapman & Roberts 1997). The background extinction rate is between 1 and 7 species per year (Jeffries 1997), yet there have been 5 mass extinction events and eleven further major declines in the last 6 million years (Harrison 1997). The extinction rate during these mass holocausts may be between 15 and 30 species per year, yet some estimates put current extinction rates at 4000 species per year (Chapman & Roberts 1997, Jeffries 1997). We are living in, and fuelling, the sixth extinction event: some 50% of species could be annihilated in the 21st century (Morell 1999).
The cause of mass extinctions is the subject of much debate. Some researchers believe a meteorite impact caused the Cretaceous extinction, yet Hallam & Wignall (1999) suggest all five events were prompted by eustatic sea-level rise. Other possible causes are global cooling, volcanic eruptions, or the Pangaean super-continent exposing species to over-intense competition (Harrison 1997).
EVENT
Ordovician
Devonian
Permian
WHEN?
Triassic
Cretaceous
440 million years ago
370 million years ago
250 million years ago
CONSEQUENCES
210 million years ago
65 million years ago
25% of families lost
19% of families lost
54% of families lost; the most catastrophic loss of life thus far; extinction of trilobites; perhaps 90% of all pre-existing species wiped out
23% of families lost
17% of families lost; dinosaurs extinct; up to 75% of species killed off
Table 1: The 5 mass extinction events, from information in Harrison (1997) and Morell (1999).
In Hallam & Wignall (1999), species decline is theorised to have started by sea-level change causing extinction on the continental shelf; yet the authors accept that, in the case of the Cretaceous event, meteorite impact may have delivered the final coup de grâce. This is an important concept, and one which runs consistently throughout the literature: species decline is almost certainly not caused by single processes, but rather by a chain of disturbances which ecosystems cannot withstand. For instance, the population collapse of amphibians since the 1970s is ultimately blamed on habitat loss, but other factors (over-collecting, increased UV-B radiation, pathogen epidemics, etc) act in concert to precipitate the decline (Corser 2001).
No two species can live side by side from exactly the same resource: thus, species diversify to exploit different niches and microhabitats. Yet humans exploit every niche (Harrison 1997): human activities (habitat destruction, pollution, hunting, collection, etc) represent a relentless assault on natural ecosystems, from which there is no time to recover.
The current ecological conceptual framework is that ecosystems are dynamic systems in which change and disturbance are natural (Bengtsson et al 2000, Dale et al 2000). When disturbance exceeds its natural range of variation, however, the consequences are extreme. Humans alter the natural disturbance regimes of ecosystems and make it impossible for recovery to take place.
Table 2: natural disturbance regimes of corals (Nystrom et al 2000)
Process
Predation & grazing
Coral collapse
Bleaching
Storms
Hurricanes
Mass bleaching
Crown-of-thorns
Epidemics
Sea-level or temperature change
Spatial extent
1 -10 cm
1 m
1 m
1 -100 km
10 -1000 km
10 -1000 km
10 -1000 km
10 -1000 km
Global
Frequency
Weeks -months
Months -years
Months -years
Weeks -years
Months-decades
Years -decades
Years -decades
Months-century
Millennia
Duration
Minutes -days
Days -weeks
Days -weeks
Days
Days
Weeks -months
Months -years
Years
Millennia
In a study of coral reef resilience, Nystrom et al (2000) suggest that human activities alter the natural disturbance regimes of corals by transforming pulse events into persistent and chronic stress. Pulse disturbances include over-grazing by algae, peaks of predator populations, hurricanes, sea-surface temperature change, and so on. These events cause renewal and development in corals, yet with human pressure added in, the corals do not have time to recover. This pressure may be direct (dynamite fishing, collection by tourists, or removal for construction material) or indirect, as corals are passive receivers of the impacts of global warming, sedimentation caused by deforestation, eutrophication, and pollution (Nystrom et al 2000, Reaser et al 2000).
Biodiversity is threatened by four interacting mega-phenomena (Ayres 2000):
Human population growth
Energy and materials consumption
CO2 concentrations
Species extinctions
There is much in the literature which supports the suggestion of Ayres (2000) that mutually interacting phenomena cause environmental crises. When analysing species extinction and loss of biodiversity, therefore, we should not try and identify single causes.
5/ Trends in current research
Our knowledge of species richness is poor; of an estimated total of 30 million species, less than 2 million have been identified (Jeffries 1997). Furthermore, our knowledge of the processes of biodiversity is in its infancy (Bengtsson 2000). Research in the field is focused upon trying to understand how ecosystems will respond to environmental change, and what the impacts of species extinctions will be upon ecosystem function. Concern is raised at the rate of species decline, occurring faster than at any time in the past (Morell 1999). As May (1988) states:
"Conservation biology is a science with a time limit, with the clock ticking faster as human population increases."
5a/ Modelling in biodiversity research
Zacharias et al (2000) proposed a hierarchical approach to conserving marine biodiversity, by conceptualising structural and functional attributes at genetic, population, community, and ecosystem levels within ecological models. The authors contend that this type of framework is good for understanding the relationships between structure and process, and how those relationships change between levels. Thus, efforts to protect single species are misguided, because that approach ignores the interactions between a species and its environment (Zacharias et al 2000).
Price et al (1999) looked at the suitability of gap-phase dynamics,or patch models, for simulating the sensitivity of boreal ecosystems to climate variability. The authors identified a problem in that models use mean climate values, when in reality species presence/absence may be due to infrequent extreme climate anomalies, such as killing frost. Arguing that extreme events will increase in frequency with global warming, Price et al (2000) conclude that modelled predictions should be treated with caution; we need to find a way of incorporating climate variability within models.
Mapping patterns of biodiversity using Geographical Information Systems (GIS) and remote sensing is attempted by Roy & Tomar (2000). This type of geospatial modelling will, the authors contend, help in conservation by making continuous monitoring easier, and by providing systematic inventories of ecosystem diversity.
Cumming (2000) attempts to map biodiversity by using regression models to produce a probability surface of species distribution. Using existing data on distributions, the author modelled where it was probable that a certain species exists and concludes this approach is better than attempting logistically arduous presence/absence maps.
Shvarts et al (1995) attempt to predict future patterns of biodiversity by projecting present correlations in spatial variability in climate and biodiversity into the future. The authors conclude that species richness is strictly connected with climatic factors, with continentality and aridity the primary factors. Similarly, Smith et al (1995) model future distributions of latitudinal vegetation belts by comparing the climate simulations of four General Circulation Models (GCMs) at double present CO2 concentrations (see Table 3).
Current OSU GFDL GISS UKMO
TUNDRA 939 -302 -515 -314 -573
DESERT 3699 -619 -630 -962 -980
GRASSL 1923 380 969 694 810
DRY FOR 1816 4 608 487 1296
MESIC 5172 561 -402 120 -519
Table 3: changes in areal extent of vegetation zones (km² x 10 000). From Smith et al (1995). (OSU = Oregon State University; GFDL = Geophysical Fluid Dynamics Laboratory; GISS = Goddard Institute for Space Studies; UKMO = United Kingdom Meteorological Office)
Despite a discrepancy between wet and dry forests (GFDL and UKMO predicted losses of mesic forests, but larger increases in dry forests), the total area of forest is predicted to increase (Smith et al 1995). Since tropical forests contain the greatest biodiversity, an increase in their extent should result in an increase in species diversity; yet GCMs only predict climate conditions which could favour particular vegetation.
Duckworth et al (2000) used a model to predict the effect of climate change on European grasslands, and found that the potential for change is reduced when environmental factors other than climate are included (eg: soil type), and when vegetation is considered as a whole rather than on an individual species basis. Interactions between climate and other factors need to be incorporated into models of future biodiversity patterns.
Climate is a major control on vegetation distribution, yet other factors act in concert to influence the process. Unless an 8000-year trend is reversed, we may expect land clearance for agriculture to diminish the areal extent of forests.
5b/ Response to greenhouse-induced climate change
Dale et al (2000) look at the interplay between climate change and forest disturbance. Disturbance is seen as a natural and integral component of forest ecosystems, to which climate change is an added stress. The authors conclude that future projections of biodiversity in forests must take into account how climate controls the frequency, intensity and type of disturbance.
Similarly, Ayres & Lombardero (2000) consider the impacts of global change on pathogen and herbivore disturbance in forests, stating that even modest climate change will have large impacts because insects and pathogens have short life cycles, have high reproductive potential, and are mobile. The authors call for further research into the effect of climate variability and climatic extremes on the distribution of pathogens, and the incorporation of feedbacks into future models.
Reaser et al (2000) found that coral bleaching in 1998 was almost certainly due to global warming, as tropical sea-surface temperatures were the highest on record. Furthermore, bleaching was world-wide and thus not attributable to local stresses. Corals are good ecological canaries, because they are vulnerable to high temperatures and are among the first systems to show thermal stress. However, Reaser et al (2000) list other causes of bleaching, including sedimentation and UV-B radiation intensity.
Some papers try to simulate the effects of future climate change on ecosystems. White et al (2000) tested the sensitivity of three grassland communities to enhanced temperature and rainfall. They concluded that species-rich ecosystems were more likely to contain stress tolerant species capable of withstanding disturbance, yet communities with the same species richness performed differently in terms of productivity, due to different functional diversity. C4 plants had greater heat tolerance than C3 plants (White et al 2000).
Grayson (2000) attempted to predict future mammal distributions in the Great Basin of the U.S., by using past climates as analogues. He predicted a loss of mammal species, and an increase in xerophytic plant species, but added the proviso that current warming is due to greenhouse gas forcing, while the analogue climate was warmer due to changing solar radiation. Ungerer et al (1999) found that warming may allow the southern pine beetle to attack forests further north in the U.S., but distribution in the west is limited by lack of host trees.
De Groot et al (1995) suggest criteria for the selection of bio-indicators to assess the possible effects of climate change. Noting that Europe's landscape is already heavily fragmented, the authors suggest climate change is an additional stress which may prove too strong for ecosystems to resist. The authors propose future research is directed at finding suitable species to warn of climate change, and looking at how these climate sensitive species react to changes in temperature and rainfall.
5c/ Response to tropical deforestation and habitat loss
Deforestation is as old as agriculture. Three countries (Brazil, Indonesia, and the Congo Republic) have over 50% of global tropical forest (Harrison 1997). Yet these countries also have enormous populations, and the agricultural frontier continually threatens the forest.
Conversion of variable landscapes to monocultures by humans would almost certainly lead to decline in biodiversity, although at the local scale the relationship is not simple; communal lands in South Africa were found to contain more biodiversity than neighbouring nature reserves (Shackleton 2000).
Biodiversity is ultimately threatened by habitat destruction. Vallan (2000), however, found that amphibians in Madagascar react less sensitively to landscape fragmentation than to climatic change. In this study, the difficulty in establishing a single cause for species decline is illustrated: on further investigation, decline was shown to be due to adverse micro-climatic conditions on the edges of fragments.
Destruction of Australian rainforest has led to the highest global rates of mammal extinctions. Species surviving in the remnant pockets of forest are biologically dead: populations are so small extinction is inevitable within a few decades (Barkham 2000).
Deforestation accelerates the effect of global warming. Grace & Malhi (1999) estimate that a deforestation rate of 0.9% per year is equivalent to an efflux of 1.6-1.9 Gt of carbon. Conversion of tropical forest to farmland contributes 1-2 billion tonnes of carbon to the atmosphere. Lal (1999) analyses the effects of deforestation with regard to carbon sequestration and the greenhouse effect. Robertson et al (2000) state that no cropping systems result in a mitigation of carbon efflux. Thus, natural habitat destruction stresses species by accelerating climatic disturbance.
Duarte (2000) tested the response of a species-poor community to the removal of one species. The response was a decline in productivity in four of the six extant species: partial loss of species diversity leads to further decline in diversity within species-poor communities, confirming the insurance hypothesis that species-rich communities are more likely to withstand disturbance.
5d/ Response to stratospheric ozone depletion
If ozone within the stratosphere continues to be depleted, intense UV-B radiation will affect ecosystems in harmful ways. UV-B radiation causes vegetation to absorb less CO2 via photosynthesis, so more CO2 may accumulate in the atmosphere and cause further global warming (Lichterman 1999).
Studies have shown that enhanced UV-B radiation has a detrimental effect on plant productivity. Li Yuan et al (2000) tested 20 wheat cultivars under simulated conditions equivalent to a 20% depletion of ozone: 19 cultivars showed a negative response, indicating inhibition on growth and crop yield. Under similar conditions, Correia et al (2000) found decreases in yield and biomass production of up to 49% in maize crops.
If natural ecosystems react to enhanced UV-B radiation in the same manner, species richness may decline. We do not know the precise response to UV-B forcing, but perhaps 20% of plants are sensitive (Li Yuan et al 2000). Laakso et al (2001) suggest the effects of UV-B may be cumulative; species response to disturbance will not be abrupt, so the impacts of ozone depletion may not be apparent immediately. For animals, UV-B will cause heat stress, skin cancers, and increasing blindness through cataracts (Lichterman 1999).
5e/ Response to desertification
Investigating the hypothesis that desertification reduces species diversity in mammals, Whitford (1999) found greater mammal diversity in degraded areas than in adjacent desert grasslands. One explanation for this is that grassland species may remain in areas that become degraded, and are joined by species that prefer desertified areas. Vallan (2000) suggests that as habitat dwindles, species richness initially increases due to crowding before declining. Species richness in the areas studied by Whitford (1999) may show a decline in mammal diversity at a later date.
Whitford (1999) concludes that biodiversity is not a good measure of desertification impacts. Since all fauna rely on vegetation for food or shelter, a reduction in soil fertility and consequent decline in vegetation cover can be expected to cause a decline in species richness.
6/ Proposals for future research
The study of environmental change is a new science; there are many feedbacks and interactions between components of the biosphere and atmosphere that we do not understand. Loss of biodiversity may cause great harm to natural and human ecosystems: it is imperative that future research explains the role of biodiversity in ecosystem productivity, and illustrates the danger to humankind of biodiversity depletion.
Usher (2001) calls for more interdisciplinary studies, and many of the articles researched for this report conclude by emphasising the need for refined predictions of future change from allied disciplines. Ayres & Lombardero (2000) list 13 proposals for future research, especially on the interactions and feedbacks between biota and climate. Bengtsson et al (2000) call for more research into the role of biodiversity in ecosystem function and stability, studies of population dynamics, and field tests of the insurance hypothesis. De Groot et al (1995) look for the identification of indicator species which warn of future climate change.
An understanding of the link between biodiversity and ecosystem productivity will show the true value of biodiversity, and refined methods of projecting future patterns of biodiversity may assist in conservation efforts. A shift in emphasis from conservation of single species to protection of ecosystem diversity is a more effective way of protecting biodiversity. We need to move away from disputable aesthetic campaigns for species conservation, and establish the real scientific threat to humankind that the loss of biodiversity represents.
7/ Conclusions
Our knowledge of the processes and value of biodiversity is sketchy, perhaps because it is difficult to observe or measure biotic interactions such as predation and competition. We know more about the causes of species decline, but must not jump to conclusions and blame all ills on individual causes. As the research shows, species response to change is complicated by a number of factors and feedback mechanisms.
It is crucial that we establish the true value of biodiversity to humankind. We need to react now to a changing global environment, and understand the threat posed by the loss of biodiversity. ENDS (3486 words)
References:
Ayres E. (2000) ‘The Four Spikes’ Futures 32, pp 539-554.
Ayres M & Lombardero M. (2000) ‘Assessing the consequences of global change for forest disturbance from herbivores and pathogens’ The Science of the Total Environment 262, pp263-286.
BarkhamP. (2000) ‘Reckless bush clearance may cost Australia the earth’ The Guardian 24/11/2000.
Bengtsson J, Nilsson S, Franc A & Menozzi P. (2000) ‘Biodiversity, disturbances, ecosystem function and management of European forests’ Forest Ecology & Management 132, pp39-50.
Chapman J & Roberts M. (1997)‘Biodiversity: The Abundance Of Life’. Cambridge.
Correia C, Coutinho J, Bjorn L & Torres-Pereira J. (2000) ‘Ultraviolet-B radiation and nitrogen effects on growth and yield of maize under Mediterranean field conditions’ European Journal of Agronomy 12, pp117-125.
Corser J. (2001) ‘Decline of disjunct green salamander (Aneides aeneus) populations in the southern Appalachians’ Biological Conservation 97, pp119-126.
Cumming G. (2000) ‘Using habitat models to map diversity: pan-African species richness of ticks (Acari: Ixodida)’ Journal of Biogeography Vol 27 (2) pp425-440.
Dale V, Joyce L, McNulty S & Neilson R. (2000) ‘The interplay between climate change, forests, and disturbances’ The Science of the Total Environment 262, pp201-204.
De Groot R, Ketner P & Ovaa A. (1995) ‘Selection and use of bio-indicators to assess the possible effects of climate change in Europe’ Journal of Biogeography Vol 22 pp 935-943.
Duarte C. (2000) ‘Marine biodiversity and ecosystem services: an elusive link’ Journal of Experimental Marine Biology and Ecology 250, pp 117-131.
Duckworth J, Bunce R & Malloch A. (2000) ‘Modelling the potential effects of climate change on calcareous grasslands in Atlantic Europe’ Journal of Biogeography Vol 27 (2) pp347-358.
Grace J & Malhi Y. (1999) ‘The role of rainforests in the global carbon cycle’ Progress in Environmental Science Vol 1, No. 2 pp177-193.
Grayson D. (2000) ‘Mammalian responses to Middle Holocene climatic change in the Great Basin of the western United States’ Journal of Biogeography Vol 27, No.1 pp 181-192.
Hallam A & Wignall P. (1999) ‘Mass extinctions and sea-level changes’ Earth-Science Reviews 48, pp217-250.
Harrison P. (1997) ‘The third revolution’. Penguin.
Ives A, Klug J & Gross K. (2000) ‘Stability and species richness in complex communities’ Ecology Letters 3, pp399-411.
Jeffries M. (1997) ‘Biodiversity and Conservation’. Routledge.
Laakso K, Kinnunen H & Huttunen S. (2001) ‘The glutathione status of mature Scots pines during the third season of UV-B radiation exposure’ Environmental Pollution 111, pp349-354.
Lal R (1999) ‘Soil management and restoration for C sequestration to mitigate the accelerated greenhouse effect’ Progress in Environmental Science Vol 1, No.4 pp307-326.
Lichterman J. (1999) ‘Disasters to come’ Futures 31, pp593-607.
Li Yuan, Zu Yanqun, Chen Haiyan, Chen Jianjun & Yang Jilong (2000) ‘Intraspecific responses in crop growth and yield of 20 wheat cultivars to enhanced ultraviolet-B radiation under field conditions’ Field Crops Research 67, pp25-33.
May R. (1988) ‘How many species are there on Earth?’ Science 241 pp 1441-49.
Morell V. (1999) ‘The Sixth Extinction’ National Geographic Vol 195, No.2 pp42-56.
Nystrom M, Folke C & Moberg F. (2000) ‘Coral reef disturbance and resilience in a human-dominated environment’ Tree 15, no 15 October 2000, pp 413-419.
Price D, Halliwell D, Apps M & Peng C. (1999) ‘Adapting a patch model to simulate the sensitivity of Central-Canadian boreal ecosystems to climate variability’ Journal of Biogeography 26 (5) pp1101-1113.
Reaser J, Pomerance R & Thomas P. (2000) ‘Coral bleaching and global climate change: scientific findings and policy recommendations’ Conservation Biology 14 (5) pp1500-1511.
Robertson G, Paul E & Harwood R. (2000) ‘Greenhouse gases in intensive agriculture: contributions of individual gases to the radiative forcing of the atmosphere’ Science 289 pp 1922-25.
Roy P & Tomar S. (2000) ‘Biodiversity characterization at landscape level using geospatial modelling techniques’ Biological Conservation 95, pp95-109.
Shackleton C. (2000) ‘Comparison of plant diversity in protected and communal lands in the Bushbuckridge lowveld savanna, South Africa’ Biological Conservation 94, pp273-285.
Shvarts E, Pushkaryov S, Krever V & Ostrovsky M. (1995) ‘Geography of mammal diversity and searching for ways to predict global changes in biodiversity’ Journal of Biogeography Vol 22, pp907-914.
Smith T, Halpin P, Shugart H & Secrett C. (1995) ‘Global Forests’ in ‘As Climate Changes (Strzepek K & Smith J., eds). Cambridge.
Ungerer M, Ayres M & Lombardero M. (1999) ‘Climate and the northern distribution limits of Dendroctonus frontalis Zimmerman (Coleoptera: Scolytidae)’ Journal of Biogeography 26 (6) pp1133-1145
Usher M. (2001) ‘Landscape sensitivity: from theory to practice’ Catena 42, pp375-383.
Vallan D. (2000) ‘Influence of forest fragmentation on amphibian diversity in the nature reserve of Ambohitantely, highland Madagascar’ Biological Conservation 96, pp31-43.
Van Straalen N. (1999) ‘Developments in genetic biodiversity in toxicant-stressed populations’ Progress in Environmental Science 1 (2) pp195-201.
Whitford W. (1999) ‘Desertification and animal biodiversity in the desert grasslands of North America’ Tektran/US Department of Agriculture
White T, Campbell B, Kemp P & Hunt C. (2000) ‘Sensitivity of three grassland communities to simulated extreme temperature and rainfall events’ Global Change Biology 6, pp671-684.
Zacharias M & Roff J. (2000) ‘A hierarchical ecological approach to conserving marine biodiversity’ Conservation Biology 14 (5) pp1327-1334.
