The Threat of Climate Change to Freshwater Pearl Mussel Populations

ReportArticle Lee C. Hastie, Peter J. Cosgrove, Noranne Ellis and Martin J. Gaywood The Threat of Climate Change to Freshwater Pearl Mussel Populations and a number of important populations may be threatened by Changes in climate are occurring around the world and the these changes. For example, large floods have been shown to effects on ecosystems will vary, depending on the extent adversely affect mussels (10), and although these stochastic and nature of these changes. In northern Europe, experts events were historically rare, there is evidence to suggest that predict that annual rainfall will increase significantly, along they may now be occurring more often as a result of climate with dramatic storm events and flooding in the next 50– change (9). Populations may also be detrimentally affected by a 100 years. Scotland is a stronghold of the endangered number of other climatic factors, including changes in tempera- freshwater pearl mussel, Margaritifera margaritifera (L.), and a number of populations may be threatened. For ture, sea level, habitat availability, host fish stocks and human example, large floods have been shown to adversely affect activity. mussels, and although these stochastic events were In this paper, we investigate the direct and indirect threats historically rare, they may now be occurring more often as posed by suggested climate scenarios for the present century, and a result of climate change. Populations may also be discuss the general implications for the conservation manage- affected by a number of other factors, including predicted ment of threatened M. margaritifera populations and their habi- changes in temperature, sea level, habitat availability, host tats. fish stocks and human activity. In this paper, we explain how climate change may impact M. margaritifera and discuss the general implications for the conservation THE FRESHWATER PEARL MUSSEL LIFE CYCLE management of this species. Margaritifera margaritifera is one of the longest-lived inverte- brates known, capable of reaching ages > 100 yrs (11). In com- mon with other freshwater bivalves, it is typically dioecious, with both sexes maturing at age 12–20 yrs (12). An annual cycle of INTRODUCTION gametogenesis is apparent (4). Fertilization is external and oc- During the past 100 years, the freshwater pearl mussel, curs in early summer; the female mussels inhale sperm by nor- Margaritifera margaritifera (L.), has declined throughout its mal filtering action. In mid-late summer, following an incuba- holarctic range to the extent that it is now listed by IUCN as an tion period of several weeks, the females discharge their larvae endangered species (1). The main causes are considered to be (glochidia) into the river. Glochidia, which resemble miniature gross industrial and agricultural (organic) pollution, over- mussels (measuring 0.06–0.08 mm across: 13), are obligate para- exploitation by pearl fishermen, decline of salmonid host stocks sites of fish, usually found encysted on the gills and/or fins of and physical riverbed habitat degradation due to hydroelectric their hosts. Margaritiferid glochidia are associated with operations and river management schemes (2). Margaritifera salmonids; those of M. margaritifera can only complete their de- margaritifera is now protected in Britain under the UK Wild- velopment on the gills of Atlantic salmon, Salmo salar (L.) or life and Countryside Act 1981. It is also listed on Appendix III brown trout, Salmo trutta (L.). A few glochidia are ingested or of the Bern Convention and Annexes II and V of the EC Habi- inhaled by host fish and manage to attach to and encyst on their tats Directive. Annex II lists species of community interest whose gills. In M. margaritifera, the parasitic phase lasts for several conservation requires the designation of Special Areas of Con- months before the glochidia metamorphose into tiny mussels (by servation (SACs), and Annex V lists species whose exploitation then ~ 0.4 mm across), excyst from the host gills and drop off must be subject to management (although pearl fishing is now and settle onto the riverbed (12). Those that settle in clean, sta- banned completely in most countries). In the UK, it is also listed ble sand (recruits) may survive to adulthood. A diagram of the under the Biodiversity Action Plan as a ’Priority Species’ requir- complete M. margaritifera life cycle is provided in Figure 1. ing the development and implementation of a Species Action Plan dedicated to its survival. CLIMATIC FACTORS LIKELY TO AFFECT MUSSEL There is no doubt that remaining populations are now better POPULATIONS protected by widespread bans on pearl fishing, stronger pollution control measures and restrictions on river engineering ac- Temperature tivity (3). However, in addition to potential problems with Changes in temperature may influence a number of factors that salmonid host stocks (4), it is likely that climate change will pose are important to survival, including individual growth, longev- a serious new threat to the survival of a number of M. margariti- ity and reproductive success (11, 14). Margaritifera marga- fera populations over a large part of its range. ritifera is a holarctic species that is patchily distributed in north- It is now widely accepted that changes in climate are occur- western Europe and northeastern North America, between 40°N ring around the world (5) and that the effects on different eco- and 70°N (1). In Scotland, which is situated well within this lati- systems will vary (e.g. 6–8). In northern Europe, the most re- tudinal range (55–60°N), the temperatures of small streams sup- cent and conservative estimates predict that annual rainfall will porting mussel populations can vary from 0–25°C in some years increase significantly, along with storm events and large-scale (unpubl. data), so this species exhibits a considerable degree of flooding in the next 50–100 years (5). In northwestern Scotland, thermal tolerance. there is evidence that significant changes in the hydrological During the 20th century, the global mean air surface tempera- behavior of rivers occurred during the late 1980s (9). The riv- ture warmed by 0.3–0.6°C with Europe experiencing warming ers in this area are a global stronghold of M. margaritifera (2), above the global average at 0.8°C (15). Sometime around the 40 © Royal Swedish Academy of Sciences 2003 Ambio Vol. 32 No. 1, Feb. 2003 http://www.ambio.kva.se example, the expected increases in maximum temperatures and the frequency and duration of exceptionally warm periods in summer may be detrimental, particularly to mussels in small streams (which tend to heat up rapidly). At present, the critical upper thermal limits for survival and normal functioning in this species are unknown. A number of studies have indicated that the timing of reproduction in M. margaritifera is influenced by temperature—mussels tend to spawn earlier in warm conditions (22). This has also been reported for the closely-related M. falcata in North America FERTILIZATION (23). According to Ross (24), annual spawnings of M. marga- fertilized eggs develop within female ritifera may vary by several months, due to thermal effects. The timing of mussel and host fish reproductive cycles may be linked—in Scottish rivers, for example, mussels spawn when salmon and trout fry are abundant (12). Differential effects of temperature change may cause problems by uncoupling the timing of mussel and salmonid reproduction. Changes in host fish availability and other possible indirect effects of climate change are discussed later. Figure 1. The freshwater pearl mussel life cycle. Precipitation (Quantitative data from ref. 12). The consequent increase in evaporation and alterations in air mass circulation also increases cloud cover. This was most marked across the west coast of Scotland where the average mean daily hours of bright sunshine decreased between 1941– Table 1. Climate change scenarios for Scotland for the 30-yr periods centered on the 2020s and 2050s with respect to the 1971 and 1964–1993 by around 16% (25). Although the North- 1961–1990 average (16), and sea level rise projections for ern Hemisphere only saw an increase in precipitation levels of Scotland (17). around 1% (26), Scotland experienced much higher increases. The most extreme cases of increasing precipitation levels were Year Temperature Precipitation CO2 Sea level (°C) (%) (ppmv) (m) in the west during the winter months, increasing by up to 15– 20% between 1941–1971 and 1964–1993 (27). The Loch Ran- 1990 —— —— 353 —— 2020s +0.5 → +1.2 +3 → +6 415 → 434 —— noch area experienced an increase of 57–58% more rain during 2050s +0.8 → +2.0 +3 → +5 467 → 528 +0.08 → +0.72 March between 1916–1950 and 1961–1990 (27). Some of this rain has been experienced as greater storm events (9), which also alter the habitat structure of mussel beds (10). A close match between historical precipitation (rainfall) and 2020s (i.e. 2010–2039) it is possible that Scotland will witness M. margaritifera recruitment patterns (1957–1991) was observed a 1°C increase in mean air surface temperature and a 2°C rise in the River Kerry, northwestern Scotland (Fig. 2). In general, sometime around the 2050s (i.e. 2040–2069) (Table 1). These the mussels appeared to recruit well during wet years and vice figures are based on global circulation models published in 1996 versa. With annual average increases in precipitation expected (5) that have since been revised upward to predict a global warm- to be about 3–6% over the next five decades (Table 1), there is ing of between 1.4°C and 5.8°C (18). How this will affect the no evidence to suggest that recruitment in the Kerry population hydrothermal regimes of rivers is not known as there is a dearth is threatened by an overall increase in rainfall in this time.

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