Although there may be obvious impacts of climate change in marine systems, other effects may be more insidious and difficult to monitor or to assess. The aim of this paper is to present the scientific basis for such a scenario and specifically to consider the potential impact of climate change on the reproduction of marine invertebrates with regard to the implications for migrating bird populations on the Humber estuary in northeast England. This will be illustrated using several case studies, mostly taken from the Polychaeta, most of them representing prey organisms in the coastal food chain. See the Glossary for an explanation of specialized terms.
Environmental cues control or synchronize the reproductive cycle of many marine invertebrates. Of these environmental cues, photoperiod and temperature have been shown to moderate reproduction either individually or in combination. In addition, they may act directly or, in the case of photoperiod, set circannual clock mechanisms. These environmental cues may affect a number of reproductive parameters, including sex determination, gametogenesis and spawning. Gonadotrophic and spawning hormones appear to act as the transducers between the environment and the gamete, and limited evidence indicates that temperature and photoperiod can alter levels of these. Such processes occur in a range of estuarine invertebrates that constitute important components of the diets of overwintering birds. Global warming is likely to uncouple and alter the phase relationship between temperature and photoperiod and this is likely to have significant consequences for animals that develop gametes during the winter and spawn in the spring in temperate northern latitudes. Species that cue reproduction to photoperiod are likely to be particularly vulnerable. Although this is unlikely to lead to extinctions, it may cause local extirpations. However, this will depend on speed of adaptation to changing climate in relation to speed of climate change and the degree of mixing between populations across the range of the species. More likely will be significant impacts on fecundity, spawning success and recruitment, and this may have significant implications for overwintering birds of national and international importance, and, ultimately, on the conservation status of estuaries such as the Humber in the UK.
STATUS OF BIRDS ON THE HUMBER ESTUARY
The Humber estuary is an internationally important site for birds, holding 1% of the individuals of several internationally important species of wildfowl and wader that use the intertidal flats and saltmarshes during the winter (Ramsar Convention Bureau 1990, Heath & Evans 2000). In addition, it is of national importance for several other species using criteria developed by Pollit et al. (2000). It has been designated a Special Protected Area (SPA) under the Wild Birds Directive with further protection given under the Habitats Directive. SPA designation is based on the presence and numbers of many of the birds shown in Table 1, together with breeding Little Tern Sterna albifrons, and wintering populations of Hen Harrier Circus cyaneus, Common Teal Anas crecca, Mallard A. platyrhynchos and Eurasian Oystercatcher Haematopus ostralegus. It is also a Ramsar site (English Nature 2000) and several of the intertidal mudflats are designated as Sites of Special Scientific Interest (SSSI) under the Wildlife and Countryside Act (IECS 2002).
|Species||Winter peak||International threshold||National threshold||Population importance|
|Shelduck*Tadorna tadorna||4 682||3 000||750||International|
|Golden Plover*Pluvialis apricaria||36 674||18 000||2 500||International|
|Grey Plover*Pluvialis squatarola||1 704||1 500||430||International|
|Lapwing*Vanellus vanellus||36 305||20 000||20 000||International|
|Knot*Calidris cautus||28 591||3 500||2 900||International|
|Dunlin*||24 657||14 000||5 300||International|
|Bar-tailed Godwit*||2 339||1 000||530||International|
|Redshank*Tringa totanus||4 306||1 500||1 100||International|
|Dark-bellied Brent Goose*Branta bernicla||2 348||3 000||1 000||National|
|Eurasian Wigeon Anas penelope||5 678||12 500||2 800||National|
|Common Pochard Aythya ferina||940||3 500||440||National|
|Scaup Aythya marila||198||3 100||110||National|
|Goldeneye Buchephala clangula||423||3 000||170||National|
|Ringed Plover*Charadrius hiaticula||357||500||290||National|
|Sanderling*Calidris alba||493||1 000||230||National|
|Black-tailed Godwit Limosa limosa||495||700||70||National|
|Curlew*Numenius arquata||2 830||3 500||1 200||National|
PRINCIPAL FOOD COMPONENTS AVAILABLE TO OVERWINTERING BIRDS
On some estuaries, gammarids can be among the main prey items of the Eurasian Oystercatcher, Common Eider Somateria molissima, gulls and Ruddy Turnstone Arenaria interpres (McLusky 1989). However, the preferred prey of many birds varies with time of year, age and sex. Adult Oystercatchers may feed on Mytilus edulis, Littorina littorea, Nereis diversicolor and Scrobicularia plana (Boates & Goss-Custard 1992). However, males may feed mainly on M. balthica, whereas females prefer N. diversicolor (Ens et al. 1996). Oystercatchers also seem to switch between surface prey, such as N. diversicolor, to deep living prey, such as M. balthica in the spring and autumn (Zwarts et al. 1996). Black-headed Gulls Larus ridibundus prey mainly on N. diversicolor in the summer, and S. plana in the winter as well as on Hydrobia ulvae and Carcinus maenas (Moreira 1995). Dunlin Calidris alpina in the Wadden Sea feed almost exclusively on polychaetes during spring with a higher proportion of shrimps, Crangon crangon, taken in late summer (Nehls & Tiedemann 1993). Bar-tailed Godwits Limosa lapponica prey on about 17 different species, including Arenicola marina, N. diversicolor, Nephtys hombergii, Scoloplos armiger and C. maenas. However, during the winter N. diversicolor, Nephtys hombergii and Scoloplos armiger constitute approximately 99% of their prey (Scheiffarth 2001).
The importance of estuaries as migratory stopovers is therefore clearly linked to productivity and the numbers and biomass of invertebrates available as food. These food supplies can be divided into three main phyla, of which the Polychaeta appear to be the most important, although both molluscs and crustaceans have significant value (Table 2). Any climatic impact on this secondary production may therefore have severe consequences for migrating birds and one way in which this may occur is through impacts in invertebrate reproduction.
|Species||Unidentified items||Worms||Crabs||Cockles||Small clams||Large clams|
ENVIRONMENTAL AND ENDOCRINE CONTROL OF MARINE INVERTEBRATE REPRODUCTION
Reproduction in marine invertebrates must be highly synchronized to ensure success. Ultimately, this synchronization is at the level of gamete development and spawning between individuals in a population. However, prior to this it may also involve pair formation or the preferential birth and growth of a particular sex to ensure successful size-selective mating. This synchronization is moderated using external cues and for many species temperature and photoperiod are the principal variables to which the organism's biology can be linked. These may act either directly or indirectly to reset or maintain internal clock mechanisms. However, evidence increasingly shows that transduction of the environmental cues to the gamete is via the endocrine system (Fig. 1) (Olive et al. 1990, Bentley & Pacey 1992, Lawrence 1996).
Environmental cues are fundamentally important in ensuring that larvae are released or develop during periods of abundant food supply (Lawrence 1996, Rees 1997). This is achieved by linking aspects of reproduction to the seasonal cycle of temperature and/or photoperiod, two fundamental physical factors that also influence biological cycles such as phytoplankton production.
Of the two variables, photoperiod is the more reliable cue. Synchronization to this ensures that aspects of an individual's physiology are specifically linked to time of year. Temperature, although showing an annual cycle of change, can also vary between years and seasons. If a temperature threshold or change is used as the single cue, this may result in the animal initiating a physiological response at the wrong time in relation to calendar date.
The following case studies are presented to illustrate the linkage between temperature and photoperiod with invertebrate reproduction and the potential impacts of climate change on these processes.
ENVIRONMENTAL SEX DETERMINATION (ESD) IN GAMMARUS DUEBENI
The sex of many species is determined by environmental factors and in these species the cues appear to act on the embryo during development. Sex determination should therefore be linked with a variable that has a predictable annual cycle and should reflect future sex-specific size-related fitness (Naylor et al. 1988). Turtles and other reptiles, for example, show temperature-dependent sex determination (TSD). Offspring of turtle eggs incubated under high temperatures are biased toward females whereas under lower temperatures males are predominantly produced (Graves & Reavey 1996).
Several species of estuarine amphipod, including Gammarus duebeni and G. lawrencianus, show ESD. However, in G. duebeni, the proximate cue appears to be photoperiod although this may be temperature compensated.
The clarity of the ESD signal in G. duebeni is linked with geographical location. In these populations males are preferentially produced early in the year from overwintering eggs. The first offspring are released in April and pass the critical developmental stage in May. This occurs under a long day photoperiod and offspring are predominantly male. Under short daylengths, the sex ratio of broods becomes biased toward females (Naylor et al. 1988). This gives the males significantly longer to grow and size-related fitness is linked with the mating process and precopula pair formation.
However, photoperiod may not be the only cue by which G. duebeni sex is determined. In some populations, males in the field may be produced under short day conditions in contrast to laboratory-reared animals. This indicates that some other factor, probably temperature, might play a role in sex determination (Watt & Adams 1993). Furthermore, preliminary evidence has also been presented to indicate a genetic component to the process (Watt 1994).
Temperature is involved in the seasonal cycle of egg production in G. duebeni and G. insensibilis (Sheader 1983, 1996). In both species, larger eggs are produced during the winter but greater numbers of smaller eggs are produced during the summer. Sheader (1996) identified a clear inverse relationship between egg size and temperature, which was related to the length of the winter intermoult. Although this might appear to indicate a relationship between temperature, photoperiod, egg size and sex of offspring in gammarids, evidence does not currently support any link between these factors (Dunn et al. 1996).
The mechanism of sex determination in G. duebeni is unknown. However, it possibly involves production and release of hormones that trigger genes for specific sex characters in the developing embryo. Sex steroid hormones appear to be involved in TSD in reptiles (Crews 1996, Flemming et al. 1999). Alternatively, sex determination may be linked to maternally transmitted parasitic sex factors (PSFs), as has been described in the closely related isopod Armadillidium vulgare (Jachault et al. 1992). In these, the PSF seems to reverse genetic males into functional neo-females. Parasitic sex determination and an intersex condition have been described in G. duebeni and it has been suggested that intersex may also be a cost of ESD in this species (Dunn et al. 1994, 1996).
TIMING OF REPRODUCTION IN POLYCHAETA
The timing of reproduction in marine and estuarine invertebrates is highly complex. To illustrate this, the reproduction of five species will be considered; Nereis virens, N. diversicolor, Harmothoe imbricata, Nephtys hombergii and Eulalia viridis. These species differ in their life history (semelparity or iteroparity), type of ovary, method of vitellogenesis, hormonal control system and response to temperature and photoperiod cues.
N. virens and N. diversicolor
Nereidae are semelparous. Gametes are developed and released once in a lifetime, after which the adult dies. In these animals the synchronous timing of reproduction is crucial and must be tightly controlled, not only within the individual but also across the population. Temperature and photoperiod both influence the gametogenic process in the nereids. For example, it has been shown that in populations of N. virens from northeast England, low temperatures (7–12 °C) encourage oocyte growth whereas high temperatures inhibited growth (Rees 1997). However, photoperiod is equally important with short daylength (light–dark (L : D) 8 : 16 h) promoting oocyte growth and long days (L : D 16 : 8 h) inhibiting it. Furthermore, the switch to short winter daylengths can initiate oocyte development in this species (Last 1999).
In addition, female N. virens can be induced to produce new oocytes at any time of the year through photoperiod and/or temperature changes, whereas vitellogenesis can only be induced by switching the animals to short day photoperiod (Rees & Olive 1999). However, N. virens also need to be exposed to long daylengths to achieve successful fertilization and larval development (Rees 1997).
Temperature has also been linked with spawning in nereids. For example, N. diversicolor spawn in the spring after a period of low winter temperatures. Temperatures above 6 °C induced gamete maturation and approximately 4 weeks later, as temperatures reach 12 °C, the individuals spawn (Bartels-Hardege & Zeeck 1990). Spawning is asynchronous in animals maintained under constant high temperature and it seems that the rise in temperature from winter to early spring is highly important in aiding the synchronization of gamete maturation and spawning (Bartels-Hardege & Zeeck 1990). Further synchrony is imposed in the spawning of N. diversicolor, as mature animals only release their gametes in synchrony with the semilunar cycle. At the time of gamete maturation, many Nereidae undergo metamorphosis to an epitokous form, although N. diversicolor is an exception to this. These spawn in the atokous form, do not swarm and produce benthic larvae (Bartels-Hardege & Zeeck 1990).
Although these studies show clear interaction between temperature, photoperiod and, in some instances, lunar periodicity, it should be noted that the precise interaction between these cues will be specific to a particular population within the range of the species. Thus individual populations may breed at different, locally appropriate, times while using the same cues to synchronize the cycle.
The current consensus on the endocrine control of growth and reproduction in nereids is that the supraoesophageal ganglion secretes a juvenile hormone termed Nereidine. A high concentration of Nereidine in the juvenile appears to promote growth and regeneration but inhibit sexual maturation. As the animal ages, it has been suggested that there is a staged decline in the circulating hormone titre (Durchon & Porchet 1971). Growth is slowed and the ability of the animal to regenerate is lost, whereas sexual maturation is allowed to proceed. The development of the gametes is stage specific and as such there may be biochemical stages to gametogenesis that can only proceed in a definite endocrine milieu (Franke & Pfannensteil 1984). It has therefore been suggested that environmental cues trigger hormone decline, and that spawning ultimately results in response to one of these cues.
Oogenesis in Nereidae can be divided into four stages: previtellogenesis, vitellogenesis, corticogenesis and maturity (Dhainault 1984). High concentrations of Nereidine permit the accumulation of oogonia in the coelom (previtellogenesis) and lunar periodicity controls the release of hormone in Platynereis dumerilii (Hauenschild 1960). Originally, Dhainault (1984) suggested that the hormone promoted synthesis of RNA and autosynthetic yolk production. However, following the discovery that vitellogenesis in Nereidae is heterosynthetic, the role of the endocrine system has been re-evaluated and decerebration determined to cause the transition from heterotrophic yolk synthesis to autosynthetic corticogenesis (Porchet et al. 1989).
Most recently, it has been shown that Nereidine promotes the uptake of vitellin by developing oocytes in N. diversicolor. Using fluorescently labelled vitellin, incorporation of the protein is significantly increased in previtellogenic and mature oocytes cultured with supra-oesophageal ganglion extract from previtellogenic juveniles (Fig. 2).
H. imbricata is an iteroparous species in which two batches of eggs are produced each year. Gametogenesis begins in autumn with the first batch of oocytes undergoing vitellogenesis during the winter before being spawned in March. These oocytes are subject to photoperiod and temperature regimes that must be experienced for successful gametogenesis (Garwood 1980, Garwood & Olive 1982). Spawning is linked to calendar date, and H. imbricata exhibit a circannual reproductive cycle in which photoperiod acts as the zeitgeber and sets the clock (Garwood 1980).
Individuals must be exposed to low photoperiods of 13 h or less for a continuous period of 42–55 days for oogenesis to be successful. Falling temperatures during this period help to synchronize the gametes’ progression to maturity (Clark 1988). A final rapid growth phase is accelerated by low temperatures and long daylengths but only in those animals that have experienced at least 50 days of photoperiod below 13 h (Clark 1988). These conditions occur during the transition from winter to spring, when water temperature is still low but daylength is increasing (Bentley & Pacey 1992).
A gonadotrophic hormone that increases egg protein synthesis in developing oocytes promotes vitellogenesis in H. imbricata (Olive et al. 1990, Lawrence 1996). The hormone appears to be female specific (Lawrence 1996) and is still available to the second cohort of eggs (Bentley et al. 1994). A link between oogenesis, spawning and pheromone production has been suggested for H. imbricata. At 10 °C, significantly greater numbers of females exposed to long days spawned compared with those exposed to short days (Watson et al. 2000). Furthermore, spawning in short-day females was increased if a prostomium from a long-day female was transplanted into them. This suggests that photoperiod may increase levels of a ‘spawning hormone’ in the prostomium (Watson et al. 2000).
Nephtys hombergii and Nephtys caeca
On the northeast coast of the UK, both Nephtys hombergii and Nephtys caeca develop gametes during the winter months and spawn these during the spring. Nephtys caeca spawn successfully each year, whereas Nephtys hombergii rarely spawn completely and also suffer periodic failures to spawn despite developing a full complement of mature gametes (Olive et al. 1985). Short photoperiods increase the rate of resorption of unspawned oocytes and the onset of renewed gametogenesis. Temperature has no effect on this but low temperature does appear to be important in the production of spawning hormone, the release of which is triggered by increasing temperature (Bentley et al. 1994). A gonadotrophic hormone that accelerates oocyte protein synthesis promotes gametogenesis. The hormone is a small, heat-stable peptide that is present in the brain of males and females and that is cross-reactive between species (Lawrence 1989, Olive et al. 1990).
In E. viridis, temperature alone moderates gametogenesis although there is an endogenous component to the cycle that ultimately dictates the development of the oocytes (Olive 1980). Oogenesis and vitellogenesis are initiated in the spring with breeding occurring in the summer (Olive 1975, Franke & Pfannensteil 1984). Small oocytes are seen throughout the year, but low temperatures inhibit their development. Once sea temperature rises above 10 °C, vitellogenesis can proceed (Lawrence & Olive 1995). The progression of oocytes to maturity is temper-ature dependent, being most rapid at 20 °C and becoming progressively slower at lower temperatures, until at 5 °C it is virtually inhibited (Lawrence & Olive 1995).
Vitellogenesis only occurs under the presence of the cerebral hormone, the absence of which leads to oocyte degeneration (Olive 1975, 1976). In addition, the hormone promotes egg protein synthesis and its heterosynthetic uptake (Lawrence & Olive 1995). Furthermore, there appears to be a seasonal cycle of hormone production in relation to oocyte size (Lawrence 1996) that supports the suggestion that temperature influences the production of a vitellogenin-promoting hormone (Olive 1980).
ENVIRONMENTAL AND ENDOCRINE CONTROL OF REPRODUCTION AND SPAWNING IN MOLLUSCS
Although this paper has focused on case studies related to Polychaeta, evidence indicates that similar environmental and endocrine control mechanisms operate in the Mollusca, several of which form important parts of the diet of birds on estuaries. Table 3 summarizes the results of studies reported in the literature.
|Gametogenesis||Mytillus galloprovincialis, Pecten maximus, Pinna rugosa, Paphies donacina||Pecten maximus, M. galloprovincialis, Pinna rugosa|
|Spawning||M. edulis, Mya arenaria, Ostrea edulis, O. lurida, Pecten irradians, Teredo navalis, Gryphaea virginica, Venus mercenaria, M. recurvus, Hiatella spp., Littorina brevicula, L. littorea, Macoma balthica|
IMPACTS OF CLIMATE CHANGE ON MARINE INVERTEBRATE REPRODUCTION
Global warming will affect all biological processes, including growth and timing of reproduction. However, those species that use cues other than temperature, notably daylength, may be particularly vulnerable (Olive et al. 1990, Norse 1993, Lawrence 1996). If, for example, climate change causes a shift in the phase relationship between temperature and photoperiod this may impact on aspects of reproduction in many ways, including significant changes in sex ratio, speed or timing of gametogenesis and spawning, fecundity and, ultimately, larval survival.
The impact of climate change on gammarid sex determination has not been considered or studied. However, in other species showing ESD, evidence suggests that climate change can be significant enough to affect these processes. For example, nest populations of Painted Turtles (Chrysemys picta) with TSD show a high correlation between offspring sex ratio and mean July air temperature. Janzen (1994) implies from this that an increase in mean temperature of 2 °C may drastically skew sex ratio and an increase of 4 °C eliminate the production of males.
For this to be the case, populations exhibiting ESD would have to show altered genetic diversity, through selection for the ESD trait, and be unable to evolve fast enough to modify this in comparison with the rate of global warming. Reduced genetic polymorphism for TSD has been described in Leatherback Turtles Dermchelys coriacea (Chevalier et al. 1999) and Janzen (1994) states that genetic analysis has shown that populations may be unable to evolve fast enough to counteract the negative fitness consequences of rapid global temperature change.
Whether the same argument can be applied to gammarids is uncertain. This will depend both on the degree of isolation of any population and the speed at which the mechanism controlling ESD can evolve. The advantage for gammarids is that they have a short lifespan and reproduce annually. This contrasts significantly with turtles, which may reach ages of 30–50 years before reproducing. However, significant changes in sex ratio, as a consequence of global warming, cannot be ruled out.
The impact of global warming on gametogenesis and spawning in polychaetes is also difficult to predict. E. viridis breeds during the summer, has a planktonic larval stage and uses temperature as its proximate environmental cue. This interacts with an endogenous cycle that functions to ensure gamete competence at the correct time of year. Consequently, Lawrence (1996) has suggested that the population is likely to respond to climate change in one of three ways. They may advance their reproductive cycle in the season to coincide with earlier, increasing temperatures. Their distribution may shift poleward to remain within the normal seasonal temperature cycle, or, through genotypic adaptation, they may evolve to maintain their current position and breeding season despite changing temperature. As a result of the endogenous component of the cycle, the first of these options will only succeed if the season is not brought forward earlier than March. Furthermore, selection for individuals that make the right choice is likely to be linked with larval survival, which will depend on the timing of release coinciding with changed times of food production.
Climate change impacts on N. virens, N. diversicolor, H. imbricata and Nephtys hombergii are likely to be more complex. In each species, reduced photoperiod and low temperature is important in one or more aspects of oosorption, proper gamete development, vitellogenesis and growth, and production of spawning hormone, over the winter months.
For Nephtys hombergii, gametogenesis is influenced by photoperiod, and spawning is influenced by temperature. In H. imbricata, daylength is specifically used to set reproduction and spawning to time of year. In these and some of the Nereidae, low winter temperatures and short photoperiod are necessary for gamete development, whereas longer photoperiod (H. imbricata) and a rise in temperature (N. diversicolor) in spring are important to bring about final maturation and spawning.
The International Panel on Climate Change predicts that temperatures are likely to be 50–100% above the global mean in mid to high latitudes during the winter, precisely when nereids, Nephtys hombergii and H. imbricata require both low photoperiod and low temperature. Therefore, it seems likely that global warming may have severe consequences for these species because time of year, set by photoperiod, will become uncoupled from, and out of phase with, temperature. This may result in reduced fecundity as spawning occurs too early in the year or fewer gametes are competent to be spawned.
Synchronization of gametogenesis and spawning, within an individual and population, is critical and success relies on the interaction between temperature and photoperiod together with the transduction of these signals via gonadotrophic and spawning hormones. Consequently, there should be strong selection for individuals within the population that conform to the cycle (Olive et al. 1990).
For individual populations of species such as H. imbricata and N. virens, which use photoperiod as the proximate cue, change of location poleward may not be possible because their reproductive cycle is fixed to an annual cycle of light that is set by latitude. The ability of these to survive predicted climate change will therefore depend on the speed of genotypic adaptation in the population compared with the speed of global warming (Olive et al. 1990, Lawrence 1996) and/or the degree of mixing between individual populations. Consequently, populations of species such as N. diversicolor may be particularly vulnerable because of their lack of a planktonic larval stage and possible limited dispersal or population mixing. This, however, should be tempered by the knowledge that as a species, N. diversicolor has successfully adapted to a wide variety of temperature regimes across its broad range.
Recent evidence has shown that altered environmental conditions during the winter can have significant impacts on reproductive parameters. For example, ecological responses to the climatic effects of the North Atlantic Oscillation encompass changes in timing of reproduction, population dynamics, abundance and spatial distribution (Ottersen et al. 2001). This is further supported by reports of the consequence of unseasonable climatic events in the Baltic Sea that lead to high losses of shearwaters. These studies have highlighted the fact that marine ecosystem structure and function are intimately linked to forcing from the atmosphere (Baduini et al. 2001, Napp & Hunt 2001).
The link between climate, ecosystem structure and function may be important beyond direct climate effects. N. virens may reproduce in year 1, 2 or 3 and the animal's ability to reproduce appears to be linked with nutritional state (Rees & Olive 1999). In addition, failure to spawn in Nephtys hombergii may be a consequence of nutritional state and poor condition of adults (Olive et al. 1985). If condition and food supply affect reproductive success, any climatic impacts on these may ultimately reduce fecundity. Furthermore, larval survival will depend on the degree of match or mismatch between larval production and food availability or production cycle in the water column (Cushing & Dickson 1976). Evidence to support this is provided by Bhaud et al. (1995), who showed that short-term perturbations in temperature often on a timescale of less than 1 month may be the cause of variable reproductive success by affecting either breeding or larval success.
As the phase relationship between photoperiod and temperature becomes uncoupled by global warming, it is possible that this may have significant implications on the reproductive success of a wide range of marine and estuarine invertebrates. This possible reduction in reproductive fitness may relate to altered sex ratio in species showing ESD, to reduced fecundity as a consequence of incomplete gametogenesis, complete/partial failure to spawn or spawning at an inappropriate time, thereby reducing larval survival. Although this is unlikely to result in species extinction, it may result in extirpation of some populations that particularly cue reproduction to photoperiod. The degree to which global warming will impact on species will depend on the speed of evolution in the species to overcome reduced fitness, against the speed of global climate change and the degree of mixing between populations across the range of the species. There is limited evidence that some species, such as turtles, will not be able to evolve quickly enough to compensate for these reduced fitness traits. However, evidence for the genetic variation and fitness consequences or climate change in marine invertebrates is currently lacking and no studies have considered the speed of genotypic adaptation in these species.
However, in the first instance, it is more likely that climate change may result in a reduction in invertebrate fecundity and recruitment to an area, in species that use environmental cues to synchronize reproduction, and there is some evidence to support this. This, in turn, may impact on the biomass and secondary productivity of estuaries such as the Humber. Furthermore, many of the vulnerable invertebrates are species that constitute important components of the food for overwintering birds. Consequently, the ability of the Humber to continue to hold the numbers of birds required for it to maintain its designation as a nationally and internationally important site for birds may be at risk.
The potential impact of climate change on marine invertebrate reproduction, although not dramatic compared with predicted species extinctions, habitat loss or coral bleaching, does highlight the need to understand the physiological basis to marine structure and function together with the consequence of global climate forcing on this. The Convention on Biological Diversity commits governments to protect the world's biological resources. Increasingly, marine biologists argue that the definition of biodiversity should be expanded to include emergent properties such as ecosystem function and to highlight the conservation value of species-poor but functionally important systems such as estuaries. Evidence presented here provides further weight to that argument.
Acclimation: modification of an animal's physiology to survive changes in environmental conditions. Over a period of time, through selection, this may lead to genetic adaptation.
Atokous: a species of Nereis that does not go through epitoky.
Autosynthetic: amino acids and other constituents are taken up by the egg, which then produces large egg proteins internally.
Corticogenesis: a phase of egg development following vitellogenesis in which predominantly polysaccarides are taken up and deposited into vesicles within the egg.
Decerebration: removal of the supra-oesophageal ganglion (a small swelling at the head-end of the dorsal nerve), which may be considered the equivalent of the animal's brain.
Epitoky: a morphological transformation of the body that occurs in sexually mature nereids. This occurs in many species and allows them to swarm to the surface of the sea to spawn together.
Heterosynthetic: large egg proteins are produced externally in the coelom and taken up across the egg membrane.
Heterotrophic: has an external source of material, i.e. an egg is heterotrophic if it incorporates large egg proteins.
Iteroparous (iteroparity): a form of reproduction in which the individual will mature and reproduce several times during its life cycle, usually on an annual cycle.
Semelparous (semelparity): a form of reproduction in which the individual matures sexually, spawns and then dies, i.e. the individual only reproduces once in its lifetime.
Stolonization: a variation on epitoky in which only the hind part of the animal goes through morphological changes upon maturation. This part of the body (the stolon) then breaks free from the rest of the animal and swarms at the sea surface.
Vitellogenesis: a phase of egg development in which egg protein synthesis and deposition occur in the egg.