Climate change and ephemeral pool ecosystems: Potholes and vernal pools as potential indicator systems

Tim B. Graham
Wildlife Research Biologist, Biological Resources Division, USGS

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Introduction

Ephemeral pools can be found in many parts of the world. These pools range in size from small rock basins holding no more than 1-2 liters (Figure 1), to large vernal lakes covering hundreds of hectares (Figure 2). They occur at high elevations, below sea level, on bedrock, and on very old soils. They fill in different seasons depending on climatic patterns, and may have a single annual wet phase, or fill and dry many times a year. Most pools are heterotrophic, much of the energy passing through them comes from detritus, not direct photosynthetic production (Kuller and Gasith 1996). Pools supporting a wetland/terrestrial plant community can be considered autochthonous in that vascular plant production during the dry phase provides detritus that supports the aquatic system during the next wet phase. Some systems (e.g., rock pools and playas, Figure 3) lack significant vascular plant production, most of their energy comes from allochthonous detritus blown in or carried into the basin from the surrounding watershed, with primary production by algae in the basin varying in significance.


Figure 1. Very small pothole on the Colorado Plateau.	Figure 2. Hog lake, a large vernal lake in Tehama County, Calif.

By definition ephemeral pools dry up periodically, typically holding water for only a few days to months, yet these may represent one of the most permanent kinds of aquatic environments on Earth, judging from the age of some species that inhabit them (Fryer 1996). For example, lower Triassic tadpole shrimp fossils were assigned to the living species Triops cancriformis (Kerfoot and Lynch 1987), and Walossek (1993) recently reported finding branchiopod fossils in Cambrian rock. Despite the age of some of these groups, many branchiopods appear to be closely adapted to current climatic conditions in their pools. Cues for hatching, time to maturity, temperature tolerances, and other aspects of their ecologies are all relatively closely matched to current conditions within pools each species inhabits.

Figure 3. Aerial view of potholes in Navajo sandstone, Grand County, Utah.

Because ephemeral pools form under different climatic regimes, environmental conditions found in pools vary considerably from place to place. In a Mediterranean climate, pools are relatively cool, long-lasting environments, while under a summer monsoonal climate, pools may be fairly short-lived, warm water systems with multiple wet/dry cycles each year. Playas fill and dry slowly; the long history of mineral accumulation in these closed basins exerts a major influence on the aquatic environment in these systems. The predictability of the aquatic environment within an ephemeral pool varies considerably across climatic patterns, substrates, and geologic/geomorphic history; organisms inhabiting each pool type are well adapted to particular pool conditions. Significant changes in climate will have different impacts on different kinds of ephemeral pools, but as a group, ephemeral pools may be more sensitive to climate change than the broader landscape because they are tightly coupled to precipitation and temperature patterns.

Seasonal precipitation patterns and temperature regimes, the predictability of precipitation (intra- and inter-annual variation), chemical and physical properties of the substrate, and whether there is overland flow of precipitation before accumulating in the pools all affect the temporary pool environment. Unlike permanent bodies of water, there is no capacity to dampen out climatic fluctuations, e.g., storing water from wetter than average years that would allow continued survival of aquatic species through drier periods. Any large shift in filling and drying patterns will result in a different system, probably with retention of some species, but significant changes in community and ecosystem properties are also likely.

Ephemeral Pool Organisms

Figure 4. Adult fairy shrimp, Branchinecta packardi.

Despite the wide range of environmental conditions found in ephemeral pools around the world, there are some "universal" patterns in the structure of the macroinvertebrate communities found in these pools. Pool inhabitants are either aquatic opportunists, species that occupy both temporary and permanent waters, or specialists with precise adaptations for living in temporary aquatic environments. Ostracods are probably the most ubiquitous group in ephemeral pools, and there are usually some small planktonic crustaceans (copepods, cladocera) as well. Typically there is at least one large branchiopod crustacean, usually a fairy shrimp if a single species is present. Branchiopods (Figures 4-6) are one of the quintessential ephemeral pool groups, limited almost entirely to temporary bodies of water. Up to 8 species of branchiopods in three orders have been found in a single pool (Maeda-Martinez and Belk in press). Aquatic insects are represented by different orders depending on pool longevity, nearness to permanent water, and abundance of other invertebrates for prey. Groups usually found are diving beetles, backswimmers, water boatmen, and a variety of midges and other fly larvae.

While ephemeral pool communities have a fairly simple structure, species composition of communities varies significantly. Most pools are populated with widespread species, but some species are endemic to particular geographic regions, or pool conditions. Much of the diversity in ephemeral pools may still be undocumented, as evidenced by a recent survey of California Central Valley pools, where over 70% of the invertebrates encountered were reported from California for the first time, and over 50% may be new species (King et al. 1996).


Figure 5. Adult tadpole shrimp, Triops longicaudatus.	Figure 6. Adult clam shrimp, Leptestheria compleximanus.

Ephemeral pool organisms are faced with eventual elimination of the environment that supports them, resulting in certain death for any aquatic forms still in the pool when it dries up. Organisms that are well adapted to these habitats have some way to survive the dry phase of ephemeral pools. Usually these adaptations apply to only one stage of the life cycle, so it is important to complete their life cycle as quickly as possible so the dormant phase can be reached before the pool dries up. There is generally an emphasis on reaching sexual maturity, mating, and producing viable eggs as quickly as possible. However, predictability of the environment has affected life history characteristics of obligate ephemeral pool species, thus pools that typically last a long time have slower maturing species than those occupying smaller, shorter-lived pools.

Figure 7. Mosquito and chironomid midge larvae.

Figure 8. Spadefoot toad (Spea intermontanus) metamorph.

Adaptations that allow animals to survive the dry periods in ephemeral pools generally fall into one of three types: 1) there is a stage in the life history that can escape from the drying pool; 2) the organisms can resist desiccation in place during at least one part of its life cycle; and 3) the animals produce a desiccation tolerant stage in their life cycle. Most aquatic insects, and amphibians that use temporary pools have no specific adaptations other than the ability to leave the pool before it dries up (Figures 7 and 8). Amphibians become terrestrial, aquatic insects can fly to nearby permanent water. These animals must develop to the adult stage before they can escape, and thus may develop more rapidly than relatives in permanent water. Some invertebrates, e.g., snails and some mites (Figure 9), resist desiccation, burrowing into the substrate and sealing off their bodies with a water impervious layer (the shell and operculum of snails, the cuticle of mites). The advantage of this approach is that apparently all stages of the life cycle are capable of resistance (except snail eggs), development is suspended whenever the pool dries up, and commences as soon as the pool fills again. Because drought resisters don't have to reach a particular stage to survive the dry period, they don't have to grow as fast as other ephemeral pool inhabitants. They generally can't survive as long as desiccation tolerant organisms, and thus may be more sensitive to climatic changes. Perhaps the most intriguing adaptation to temporary aquatic habitats is that of cryptobiosis, in which organisms have at least one stage in their life cycle that can tolerate extreme desiccation, some species can lose up to 92% of their body water and still survive.

Cryptobiosis was first documented in 1702 by Anton van Leeuwenhoek, when he observed tiny "animalcules" in the sediment collected on house roofs. He dried them out then added water and found the animals began moving about again. The animals van Leeuwenhoek studied were probably free-living nematodes, which along with rotifers and tardigrades are some of the best known cryptobiotic animals. These groups are able to dry up at any stage, and typically live in terrestrial environments such as soil, moss, and tree bark. In ephemeral pools, cryptobiosis is usually limited to a single stage of an animal's life history, often the egg or cyst. Animals must complete their life cycle, from tolerant stage to tolerant stage before the pool dries up if the species is to survive.

Figure 9. Aquanothrus sp., an oribatid mite living in small potholes.

Branchiopod crustaceans are among the better known cryptobiotic species. They have cryptobiotic eggs that pass the dry phase in the pool sediment that are extremely tolerant of all kinds of adverse conditions. Planel et al. (1980) glued brine shrimp (Artemia) cysts to the outside of a spacecraft, retrieved them after the space flight and hatched viable shrimp from the cysts.


Figure 10. Hatching tadpole shrimp cyst.	Figure 11. Fairy shrimp nauplius larva (about 7 hours old).

Most branchiopods have extremely rapid early development. After the eggs are fertilized, the embryo undergoes additional development to the nauplius or metanauplius stage before entering diapause. The cryptobiotic stage is really a cyst, not an egg, in branchiopods. Under the appropriate conditions, cysts hatch (Figure 10) and the larvae begin growing and changing very fast. Figures 11 and 12 show fairy shrimp and tadpole shrimp nauplii about 7 hours after hydration. The rapid growth rate requires numerous molts (Figures 13 and 14), and quickly take on the adult form, generally by 24 hours in warm water pools (Figures 14-16). The time required to reach maturity and start producing the next generation of viable cysts (Figures 4-6) varies greatly among species, and even within the same pool, depending on genetic controls and environmental influences on these control ranges.


Figure 12. Tadpole shrimp nauplius larva (about 7 hours old).	Figure 13. Tadpole shrimp nauplius larva beginning first molt (<10 hours old).	Figure 14. Tadpole shrimp nauplius larva beginning later molt (about 15 hours old).	Figure 15. Tadpole shrimp adult (between 24 and 36 hours old).

Climatic variability occurs at a number of temporal scales, and while branchiopods are adapted to a particular range of climatic conditions at an evolutionary scale, there is intra- and interannual variation in conditions (at an ecological scale) that can also affect long term survival of a branchiopod population in a pool. For instance, if all cysts hatched the first time they got wet, a very small rain event would cause the cysts to hatch, but the pool would probably dry before the hatchlings matured and laid more eggs. Eventually, the population would be eliminated from the pool. Branchiopods deal with this inherent variability in climatic parameters by producing eggs with different diapause characteristics in each clutch. Some hatch after drying and getting wet again. Others go through more than one dry/wet cycle before they hatch. Hildrew (1985) took cysts through 9 cycles and still did not get all the cysts to hatch. It is not known what other cues operate to break dormancy in conjunction with wetting the cysts, but water temperature, changes in oxygen tension, solute concentrations, or perhaps changes in pH as the sediment is inundated may be involved for different species.

Figure 16. Adult fairy shrimp.

The old saying "Don't put all your eggs in one basket" is not heeded by pothole branchiopods. Instead, they follow Mark Twain's advice: " put all your eggs in one basket...and WATCH that basket!" Since branchiopods are forced to leave all their eggs in the one basket they develop in, they "watch" their eggs by producing different kinds of eggs, and perhaps by laying them in different parts of the pool. Not all the eggs hatch during the next hydration. This spreads the risk of eggs hatching but not being able to mature and reproduce before the pool dries again over multiple wet/dry cycles. Simovich and Hathaway (in press) demonstrated that this diversified bet-hedging was more pronounced in two species of fairy shrimp from small vernal pools in southern California where precipitation is extremely variable, than from other species that had been studied from more predictable habitats. Branchiopods are adapted to the inherent variability of climatic patterns, but shifts that are more rapid or beyond the range of "normal" variation could adversely affect the ability of a species to maintain populations in ephemeral pools.

How species deal with existing climatic variability, and potential impacts of climate change in the future are discussed for 2 types of pools: potholes of the Colorado Plateau and vernal pools of California's Mediterranean climate.

Potholes

Potholes are not erosional features of Holocene asphaltic deposits. Also known as weathering pits, they are depressions in bedrock, often with little or no watershed (Figure 17). They range in size from very small depressions holding less than a litre of water, to enormous pits over 15 m deep (Netoff et al. 1995). On the Colorado Plateau they occur primarily in sandstone, and appear to be formed by water dissolving the cement, and wind removing the loose sand from the pit (Netoff et al. 1995).

Figure 17. Aerial view of potholes in Navajo sandstone, Grand County, Utah.

Precipitation on the Colorado Plateau has a bimodal pattern, with maxima in spring and late summer (Ashcroft et al. 1992). There is high spatial and temporal variability in precipitation events, and in the quantity falling with any given storm. For pothole organisms, this translates into a very unpredictable environment; only the season when water will usually be available is fairly constant (correlating somewhat with water temperature).

On the Colorado Plateau, some species (e.g., Branchinecta packardi, Figure 4) have wide tolerance ranges (Belk 1977), and will hatch almost anytime water fills the potholes (T. Graham pers. observ.). Others are active only under warm temperatures and are usually found only following summer monsoon rains. In rare years when rain falls in May or June, these summer species will hatch much earlier than usual. The most conspicuous of these organisms are the tadpole shrimp Triops longicaudatus (Figure 5), the clam shrimp Leptestheria compleximanus (Figure 6), and the fairy shrimp Streptocephalus texanus. Under scenarios of climate change that result in an eastern shift in monsoonal rain patterns in North America, the Colorado Plateau could lose its summer precipitation and conceivably the characteristic summer pothole ecosystem if rain doesn't fall predictably when temperatures are high enough to trigger hatching.

The current variability in precipitation affects pothole ecosystems in a number of ways. For potholes near permanent water, in years of high precipitation, aquatic insects become very abundant in potholes, dispersing from streams and reproducing in potholes. This has been the situation near Moab, Utah over the past 3-4 years, where winter and spring precipitation filled potholes so full they did not evaporate during May and June before the summer monsoons hit in July. Predatory insects were able to build and maintain relatively large populations, which effectively eliminated all branchiopod crustaceans that hatched in spring or summer. Pools that usually were teeming with branchiopods in August contained only insects and ostracods. Prior to that, the area experienced years of drought during which summer rains were very low in both frequency and quantity. Branchiopods hatched, but few pools lasted long enough for the shrimp to complete their life cycles and replenish the sediment cyst bank. The combination of these weather patterns could reduce populations significantly, especially if cysts were uncommon, and/or had short lives in sediment. Fortunately, these climatic changes have not become landscape scale patterns, but they do indicate how quickly a species or group of species could be lost from these systems if precipitation and temperatures patterns change on a longer time scale.

Because of the vulnerability of branchiopods to predation, branchiopods are at risk whether precipitation increases or decreases with global climate change. The reduced precipitation (especially in summer) during the late '80's depleted the sediment cyst bank, reducing the potential size of future hatching populations by some unknown amount. The increased precipitation in the early '90's, induced more dispersal of predaceous insects, and provided long- lasting habitat that allowed their populations to build up. These insects are very efficient predators, and quickly ate any branchiopods that hatched before they could mature and produce new eggs, successful reproduction of branchiopods was again probably very limited during these years.


Figure 18. SEM photo, dorsal view, of Aquanothrus sp., an undescribed species of mite in Colorado Plateau pans.	Figure 19. SEM photo, ventral view, of Aquanothrus sp.

There is an intriguing miniature ecosystem on the Colorado Plateau found in very small weathering pits that may hold water for only a few hours to a couple days (Figure 1). In 1988, I discovered a small mite crawling in these pools (Figures 18 and 19). Dr. Roy Norton, an expert on oribatid mites, informed me it is a new species, one of only two species known in the genus Aquanothrus (Norton et al. 1997). The other species, A. montanus, is found in larger ephemeral pools in South Africa. The little pools on the Colorado Plateau also contain rotifers and other cryptobiotic organisms, but the mite is not desiccation-tolerant. It appears to resist drying out instead (T. Graham pers. observ.). As stated above, drought resisters are not as hardy as drought tolerators, and this is definitely the case with the mite. Sediment with mites held in jars for over a year yield very few if any live mites (T. Graham, pers. observ.), but rotifers in the same sediment are still alive and become active within a few minutes after getting wet. Climatic shifts that increase the time this species must be quiescent, either from reduced precipitation or increased evaporation, could affect the ability of Aquanothrus to survive on the Colorado Plateau.

Vernal Pools

Figure 20. Ephemeral snowmelt pool in the Sierra Nevada, Toulomne County, Calif.

Ephemeral pools in California vary from snowmelt pools in the Sierras to large saline playas, from coastal terraces to grassy swales in the Central Valley (Figures 20-22). The diversity of species in California temporary pools is extremely high, and includes large numbers of endemic invertebrate species (Eng et al. 1990, King et al. 1996). The pools of southern California coastal terraces and of the Central Valley are known as vernal pools because of brilliant displays of flowers (many endemic to vernal pools) that occur as the pools dry up in the spring (Figure 23). In the context of aquatic ecosystems covered here, the important season for California's pools is winter, which is the rainy season in a Mediterranean climate. Vernal pools are of particular concern because human development has destroyed most of the pools, and yet there are many endemic animal and plant species found in these pools. Some of these species are even listed as threatened or endangered under the Federal Endangered Species Act, and others have been identified as species of concern by state and federal officials. In addition, new species are being identified as surveys of remaining pools are done. Six new species of fairy shrimp have been described since 1990 (Eng et al. 1990, Fugate 1993, Thiery and Fugate 1994). A seventh species, and a new subspecies are currently being described (Denton Belk, pers. comm.). More information on California's vernal pools can be found on the California Fish and Game Natural Diversity Database Vernal Pool web page.

Precipitation in a Mediterranean climate is relatively predictable in terms of when it will occur (between November and March), but quantities vary immensely between years, and across relatively small distances. This climate, coupled with topographic variation (even at small scales, Figure 24) gives rise to a number of kinds of vernal pools, and the fairy shrimp of California at least have partitioned the vernal pool habitat, resulting in the proliferation of species, each adapted to slightly different conditions. In the Central Valley, five species of Branchinecta and Linderiella occidentalis can be found, but rarely is more than one species found in a given pool (Eng et al. 1990, D. Belk and B. Helm pers. comm.).


Figure 21. Volcanic mudflow vernal pool with clay and cobble bottom, eastern Tehama County, Calif.	Figure 22. Vernal pool with clay hardpan bottom, Vina Plains Nature Conservancy Preserve, Calif.

Figure 23. Vernal pool flowers, with different species occurring in bands related to soil moisture and temperature gradients formed as the pool dries out. Sacramento National Wildlife Refuge, Calif.

For example, B. conservatio is found in larger, longer-lasting pools that change temperature slowly through the wet season, while B. lynchi occupies adjacent smaller pools that warm more quickly. The midvalley fairy shrimp (an undescribed Branchinecta species) is found in even smaller pools that may dry and refill more than once during the rainy season. The latter species tolerates the highest temperatures, and has the shortest minimum time to maturity of any Central Valley fairy shrimp (B. Helm pers. comm.). All of these species apparently produce only one clutch of eggs each year and then die, but the midvalley fairy shrimp can produce multiple generations through a season when conditions allow additional hatches of cysts.

The quality of vernal pool environments is intimately tied to timing and amount of precipitation, and water temperature. The temperature itself is important in determining which species might hatch in a pool, but the pool must last longer, on average, than the time needed for a species to reach maturity and produce viable eggs if it is to maintain a population. Relatively small changes in precipitation timing or amount, with or without changes in temperature regime, could alter this balance. A small change in average temperature may not directly affect a species, but it could alter pool longevity enough to reduce the chances of a particular species being able to reproduce in that pool. Likewise, a shift in when rains begin to fall, even if the average amount doesn't change, could affect a species' viability simply because the water is too warm to induce hatching when it falls. Given the sensitive nature of the vernal pool fauna to environmental conditions, and the wide array of species that are adapted to slightly different conditions, vernal pools may be a very good indicator system of how global climate change is affecting Mediterranean climates.

Figure 24. Aerial view of vernal pool complex showing spatial arrangement and variety of pool sizes, Dales Lake vernal pool complex, eastern Tehama County, Calif.

Conclusions

Ephemeral pool species and ecosystems are tied directly to temperature and precipitation patterns, and thus at least have the potential to be greatly affected by climate change. Both pothole and vernal pool systems appear to be quite sensitive to climatic shifts. Individual species could be seriously affected, perhaps even driven to extinction in some cases under some predicted scenarios. These species include globally unique taxa, some with legal protection as well. We don't know enough about ephemeral ecology to understand implications beyond direct effects on species, nor do we know much about relationships between pools and their surrounding landscapes. Research is needed on cyst viability, hatching cues and other life history characteristics, tolerance ranges for various environmental parameters, ecological interactions between species, and relationships between ephemeral pools and the surrounding terrestrial ecosystems. Despite our lack of knowledge, monitoring ephemeral pool ecosystems could provide early indications of biological impacts of shifting climate, and research should be encouraged to improve our knowledge of these systems, improving our understanding of how they might react to global climate change.

Acknowledgments

I would like to thank John Gardner (Brigham Young University) for the scanning electron micrographs, Roy Norton (State University of New York, Syracuse) for the light micrographs of mites, and Todd Keeler-Wolf (California Dept. of Fish and Game) for the vernal pool pictures.

Literature Cited

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Eng, L.L., D. Belk, and C.H. Eriksen. 1990. Californian anostraca: distribution, habitat, and status. Journal of Crustacean Biology 10:247-277.

Fryer, G. 1996. Diapause, a potent force in the evolution of fresh-water crustaceans. Hydrobiologia 320:1-14.

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Maeda-Martinez, A. and D. Belk. in press. Phyllopod assemblages common to Mexico and the United States. Hydrobiologia.

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Norton, R.A., T.B. Graham, and G. Alberti. 1997. A rotifer-eating ameronothroid (Acari:Ameronothridae) mite from ephemeral pools on the Colorado Plateau. pp. 539-542. in R. Mitchell, D.J. Horn, G.R. Needham, and W.C. Welbourn (eds.) Acarology IX, Proceedings (IXth International Congress on Acarology. Ohio Biological Survey, Columbus.

Planel, H., Y. Gaubin, R. Kaiser, and B. Pianezzi. 1980. Effects of space environment on Artemia eggs. pp. 189-198. in G. Personne, P. Sargeloos, O. Roels, and E. Jaspers (eds.) The brine shrimp Artemia, Vol. I. Wettern Universa Press.

Simovich, M. and S. Hathaway. in press. Diversified bet-hedging as a reproductive strategy of some ephemeral pool anostracans (Branchiopoda). Crustacean Biology.

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