Ch. 3. Ecology of fairy shrimps life stage and species (Mertens et al. 1991). As face of the fused 12th and 13th segments of the appendages return forward from a beat, a low thorax (Fig. 1.2, p. 2). Yes, you read correctly, pressure is created between them causing water to males actually have two penes. Each lateral testis flow in (be "sucked" in) with its dead particles, empties through only the penis on its side of the and living organisms too if they are unable to body. swim against the flow. When the phyllopodia In females, oviducts extend from the ovaries beat once more, whether in graceful swimming or and enlarge at their distal ends into what are bottom scraping, increased pressure forces water called lateral pouches. These join one even through the setal meshwork and particles too large larger structure called an ovisac which also re- to pass through its pores are sieved out, whether ceives ducts from several shell glands. The living or dead, plant, animal, or mineral, nutri- ovisac expands within the brood pouch which is a tious or not. These particles are moved to a food centrally placed and posteriorly directed protru- groove between the bases of the phyllopodia, then sion from the ventral body wall of the fused geni- passed along to the jaws and mouth by specialized tal segments (Fig. 1.3, p. 3). The opening of the spiny lobes at the base of each appendage. For an ovisac to the outside is the female's genital pore, excellent discussion of anostracan feeding mech- the site that male sexual behavior is aimed at en- anisms, see Fryer (1983). tering for insemination. Rather detailed illustra- For those of you who enjoy history, it may be tions of this system can be seen in a paper by of interest to know that until just recently a fairy Brendonck (1991). shrimp's two fused genital segments were The head, the most anterior portion of the thought to be part of its abdomen because, like body, is situated immediately in front of the tho- that portion of the body, they lacked phyllopodia. rax, and bears the mandibles (jaws) and other However, certain perceptive and dogged scientists tools. Rotating action of the mandibles helps (e.g., Walossek 1993), noting that sex ducts of crush and push food into the mouth (Fryer 1966). related fossil and living branchiopods all open on The grub is moved to the teeth-like mandibles phyllopodia, that the embryology of the genital from the thoracic food groove by two pairs of segments is more similar to thoracic than ab- small head appendages located immediately be- dominal development, and that the penes of the hind the mandibles, the maxillae (Manton 1977). male are actually derived through evolutionary Unlike the teeth of humans and your pet goldfish, modification of a pair of phyllopodia, have finally but similar to a grasshopper or lobster, a fairy persuaded skeptics that the fused genital region shrimp's mandibles are not within its mouth cav- truly belongs to the thorax! That issue settled, we ity, rather they flank and ultimately cover the can now rest in peace with the notion that the mouth. Immediately anterior to the mouth, and posterior portion of the thorax is the focal point overhanging the mandibles, is a lobe or mound for the reproductive organs and their accessory called the labrum, or "upper lip", which effec- internal and external structures. tively prevents leakage from between the mandi- Internally, ovaries and testes are paired, blind bles and serves as a backstop for food that might tubules that lie alongside the gut, mainly in the otherwise be pushed further forward. This device abdomen, but in some species an anterior branch thus assures that mandibular action gets all of the extends further into the thorax as well. The food into the mouth. No messy face here! male's two penes protrude from the ventral sur- More forward yet are one pair of large,

12 Ch. 3. Ecology of fairy shrimps stalked, compound eyes and two pairs of anten- there are no arteries, capillaries, or veins, and the nae, referred to as antennules and antennae (Fig. heart is not the only propulsive force (Greene 1.3, p. 3). In males, the antennae are large, and 1924). Blood thus surrounds and bathes all body possess a variety of processes and appendages, as organs, flows out into all appendages where the well as ridges and mounds which may be orna- majority of oxygen uptake from the environment mented with spines or denticles (check out the is thought to occur, then generally moves posteri- many examples on pages 143-165). Because an- orly where it re-enters the heart via valved open- tennal shape and ornamentation apparently aid a ings called ostia. female in choosing a mature mate, such features If you want to see a thing of beauty and per- differ from species to species (Belk 1991a). As petual motion, isolate a fairy shrimp in a small might be imagined, the crafty fairy shrimp tax- volume of water (a clear-plastic box 2-4 cm across onomists have learned to use the male antennae, works fine) and observe it carefully with a magni- with their bumps, processes, and acne-like orna- fying glass or dissecting microscope. If you can mentations, as the main distinguishing character- take your eyes off the continuous motion of ap- istics of species. pendages and look inside through the thin, semi- The abdomen is continuous with the posterior transparent exoskeleton, you will not see defined end of the thorax and bears at its terminus a pair body spaces filled with blood. What you will ob- of setae-fringed, fluke-like cercopods (Fig. 7.1, p. serve above the dark, food-filled gut is the dorsal, 140). These cercopods are used in concert with elongate heart pumping rhythmically and con- abdominal musculature in turns as well as in rapid tinuously to the beat of its unseen metronome - escape locomotion much as beavers, whales, or the heart pacemaker. lobsters would employ their tails and bodies. The blood, called hemolymph, is usually col- Should you touch a cercopod you may stimulate a orless, and it contains cells, the movement of flurry of such behavior, so it seems these struc- which will allow you to trace the general direction tures serve a rear-guard sensory function as well. of blood flow (Greene 1924). At times the hemolymph may contain dissolved, not cell- Circulatory system bound, hemoglobin, which of course is a red, iron-based respiratory pigment. Because the exo- So far our discussion has dealt with fairy skeleton is so thin, this internal color makes the shrimp parts that "meet the eye". But how about animal appear reddish. Under conditions of its "innards"? We begin with the circulatory sys- plentiful oxygen hemoglobin is absent (why make tem, a fascinating component of internal structure. it if you don't have to?), but in those species hav- Unlike your closed system of blood vessels, the ing the genetic ability, hemoglobin appears to be fairy shrimp has an open circulatory system to synthesized in response to low environmental transport oxygen, digested food materials, hor- oxygen levels, allowing the animals to increase mones, and wastes through its body. The system the supply of oxygen carried to their tissues. is said to be "open" because the long, dorsal, tubu- lar heart pumps blood anteriorly into the head Oxygen: its procurement and regulation region, whence it flows posteriorly through body spaces largely under the force of muscles contract- Oxygen (02) is required for metabolic proc- ing for other body functions. In other words, esses from which energy is released to accomplish

13 Ch. 3. Ecology of fairy shrimps bodily work like locomotion, growth, egg and which are the concentration of its dissolved salts sperm production, and all that sexual activity we and, therefore, the further reduction of its 02 will speak about with biological frankness later in content - strikingly so in briny waters. The big the chapter. Aquatic creatures must not only take problem is that in the face of these reductions the in sufficient 02, but most must also maintain the consumption of oxygen by pool creatures increases rate of its intake, though some species may possi- dramatically as their metabolic rate is elevated by bly just "tough it out" in the face of a pool's de- higher temperatures. To make matters worse, creasing supply; and a reality of pool life is that atmospheric oxygen is not redistributed to the the quantity of 02 does rise and fall, sometimes pool's volume at times of atmospheric calm. drastically, even within a few hours. Oxygen, Should the habitat contain phytoplankton or sub- when in its greatest concentration in water, is pre- merged aquatic vegetation, 02 is added to the wa- sent in minuscule amounts compared to air. ter by photosynthesis during daylight hours; but at While the atmosphere contains approximately night all of the pool organisms, plants included, 200,000 parts of 02 for every million parts of air continue to consume the absolutely necessary but (ppm), water, at its maximum, is capable of dis- limited supply of dissolved oxygen. As a conse- solving only slightly less than 15 ppm, and the quence, 02 may decrease dramatically until the amount actually available dwindles from there! time "ol' Sol" begins again to brighten the morn- Scary, eh? ing sky. There is importance as well as fascination in Having said all of that, we must now advise understanding the physical and biological rela- that not much is known about how fairy shrimps tionship between the amount of 02 in an aquatic gain their oxygen and cope with drastically environment, and the latter's temperature, salin- changing concentrations. Of course most aquatic ity, and susceptibility to being mixed by wind. animals obtain 02 from the environment via gills. Remember, these factors are among the most con- Where then are the gills of fairy shrimps? We spicuous and significant actors in the dramati- have already described how the phyllopod ap- cally-changing conditions typical of temporary pendage is composed of several leaf-like lobes, waters. Before we mention the effects of these one of which has been referred to as a gill. Un- environmental agents on species, an enthusiastic doubtedly these lobes serve in the intake of oxy- discourse on their interrelatedness seems war- gen, but their combined surface-area is probably ranted. too small to account for the total volume of 02 Most temporary waters are small in volume needed by a fairy shrimp given the energetic de- and possess large surface areas compared to their mands of constant swimming. depths. These characteristics generally assure that Large enough or not, Modlin (1985) suggests the water is well mixed by wind and thus supplied that species with a propensity for greater activity with oxygen throughout. During winter and have larger gills than those which are less active. spring the atmosphere is cool and breezy, so the For example, he observed that Eubranchipus hol- pools mirror these amiable conditions, and 02 is mani, a constantly swimming, plankton-eating seldom in short supply. However, warm, calm species, has gills 1.5 times the size of those of E. days in the environs of temporary waters are not neglectus (misidentified as E. vernalis), which he uncommon, and, as the water heats at such times, suggests has a less energetic life-style because it its capacity to dissolve oxygen drops. Warming sometimes feeds by scraping the bottom sediments water also speeds up evaporation, consequences of and occasionally rests on the bottom while there. 14 Ch. 3. Ecology of fairy shrimps

Whatever the case, we believe that the surface ture through the water, but also passes water over area of the gills is still too small for sufficient 02 its respiratory surfaces thus ventilating them as intake when the fairy shrimp is faced, because of well. increasing temperature, with an escalating meta- Given these criteria for respiratory surfaces, bolic rate and scarce environmental oxygen sup- one can see why a particularly blood-rich portion plies. Why do we say this with such authority? of an appendage might be considered a gill. But Well, partly because of some limited research on take note, as did Martin (1992), that the rest of the fairy shrimps, partly because of your first author's phyllopod is also thin, as is the exoskeleton and research on aquatic insects, and partly because of epidermis of the remainder of the body, particu- the characteristics that define a respiratory sur- larly the thorax and abdomen; he concluded, face. Read on for the arguments. therefore, that these surfaces undoubtedly also Intuition tells us that a large surface area can play a role in the uptake of oxygen. We confi- allow more oxygen to pass through it per unit of dently agree with Martin's conclusion for two time than a smaller one. The hemolymph within reasons. Firstly, Gilchrist (1958, 1960) seems to the circulatory system then courses through the have demonstrated that the male of Artemia fran- gill to carry off the 02 that enters. Thinness is a ciscana, whose second antennae have very large virtue because the distance that oxygen must blade-like portions, uses these surfaces for 02 in- travel from the environment outside to the hemo- take. Secondly, Eriksen (1986) and Eriksen and lymph inside is minimized. Obviously the longer Moeur (1990) have shown that, for several aquatic it takes to move 02, via diffusion, to the circula- insects, the general body surface, particularly the tory system, the less the total amount that is abdomen, is vitally supplemental to the gills in 02 transported to the tissues in a given period of uptake. time. And of course too much cellular bulk in a No matter the extent of the respiratory sur- gill means that much of the 02 would be used faces, the ability to maintain a constant intake of within the tissues and not be carried away at all. oxygen through them in the face of a dwindling Oxygen needs to dissolve in water before it can supply (respiratory regulation) is particularly pass through a respiratory surface; therefore, such important for organisms which dwell in habitats surfaces must be moist. Maintaining moistness is whose 02 supply varies greatly throughout the not thought of as a problem for gills, of course, day. If you wonder why regulation is so impor- because only aquatic organisms possess them. tant, consider what would happen to your activity However, it helps explain why gills do not func- if your metabolism was yanked around by a dras- tion when they dry out. Finally, water containing tically changing environmental 02 supply because the needed 02 must be constantly renewed next to you could not increase or decrease your breathing the intake surface, for with use the surrounding rate in order to keep oxygen intake steady. Our supplies dwindle into insufficiency. The renewal guess is that you, and any other beast, would be at process is called ventilation, and may be actively a serious disadvantage when in competition with accomplished by the animal, or passively provided creatures who, like Energizer batteries, "just keep by the environment flowing over the organism. going , and going, and going" at a constant rate.

When you breathe, you ventilate your lungs. The The only anostracans whose 02 intake have fairy shrimp breathes by beating its phyllopodia, a been determined over a range of environmental process which not only moves our favored crea- oxygen concentrations are Branchinecta mackini,

15 Ch. 3. Ecology of fairy shrimps the alkali fairy shrimp (Eriksen & Brown 1980b), exceeding 25-30°C. and, yes, you guessed it, the brine shrimp, Ar- If indeed cool- or cold-water fairy shrimps do temia franciscana (Gilchrist 1954). Using these not usually have a problem with the environ- species as suggestive models, we can probably mental 02 supply, how is it that the few species pronounce with some "ball park" assurance that whose little lights shine in warmer water succeed fairy shrimps are respiratory regulators. You and in what must be significantly lower 02 concentra- the authors of this book regulate 02 intake by tions? Once more there are few studies and changing the rate of our breathing as our needs therefore little in the way of definitive answers, vary. Fairy shrimps undoubtedly accomplish the but in reaching for at least some educated guesses same effect by varying the beating rate of their to pass along to our readers, we return again to appendages. As useful as this ability might be Artemia the brine shrimp, Branchinecta mackini over a range of oxygen concentrations, it has its the alkali fairy shrimp, and a warm-pool anostra- limits at some genetically-determined low critical- can, the intriguing beavertail fairy shrimp Tham- level of oxygen. The particular level is "critical" nocephalus platyurus, to serve as possible models. because below that amount the animal is unable to Beginning with the last species, Hillyard and obtain enough 02 to sustain its metabolism and Vinegar (1972) noted that when pool temperatures thus its necessary activities. For adult B. mackini were great, thus dissolved oxygen low, individuals tested at 12°C, this low critical-level lies between of T. platyurus would repeatedly come to the sur- 1.4-2.9 ppm of oxygen, depending on the exigen- face where 02 was assumed to be higher "...and cies of the habitat to which the population is ac- appear to ventilate, with their respiratory append- climated. Good ol' Artemia also falls within this ages stirring the surface...." Thus when low 02 is range, 2.3 ppm, even though its test temperature a problem, behavioral responses appear to keep was about 10°C higher (23.5°C). At lower tem- fairy shrimps in the highest oxygen concentrations peratures, the critical level is undoubtedly lowered available. These same fairy shrimp enthusiasts as well because the metabolic rate, thus the de- determined that the metabolic rate of T. platyurus mand for 02, declines. However, when water is varied little with temperature change, particularly below 10-15°C, low oxygen is seldom encoun- at the warmer conditions in which they often tered. swam. Such thermal insensitivity is not at all To the contrary, when temperatures are common amongst organisms, but it does occur, higher, say 20° or 30°C, 02 is more scarce and and here we find it used to the advantage of a metabolic rate is considerably elevated, so the low warm-water fairy shrimp. critical-level of oxygen will undoubtedly be sig- More typically, metabolic rate doubles or tri- nificantly higher. Perhaps this conflict of increas- ples for each 10°C increase. Branchinecta mack- ing temperature, metabolic rate, and 02 need, in ini is known to fit this scheme. Of course, like the the face of a dwindling supply, is one of the rea- world population, metabolic rate cannot keep sons that most California fairy shrimp species doubling. At some temperature it reaches its appear during winter and spring. Among the 23 peak, then declines, and finally the animal dies. kinds of anostracans that swim in California's wet For B. mackini, its peak metabolic rate is ex- spots, only 5 might be considered "warm-water pressed around 8-10°C below its upper lethal types", that is, fairy shrimps that will not hatch temperature of about 32°C (Eriksen & Brown until water temperature exceeds about 15-17°C 1980b). Such a wide thermal span above its and which can do well as adults in temperatures metabolic maximum suggests this desert anostra- 16 Ch. 3. Ecology of fairy shrimps can, like some warm-water creatures, can "hang not been documented in all fairy shrimps, Denton tough", that is, can tolerate the increasingly less has observed red coloration at one time or another favorable conditions as temperatures rise from in a number of species and, believing its source to those which are physiologically optimal. Such a be hemoglobin, feels that most species, if not all, conclusion makes sense because this fairy shrimp can probably synthesize the pigment. If this be is one of the few California species that is occa- the case, then it appears that hemoglobin is made sionally found "doing its thing" in desert flash- and utilized only over extended periods of tough flood-formed pools during summer when toler- times as is the situation with Artemia (Gilchrist ance is undoubtedly a virtue. However, so as not 1954). Keep your checklist handy for recording to lead your thinking and conclusions astray, take such occurrences! note that Branchinecta mackini occurs over a temperature range unique among California Water, salts, and liquid wastes: their Anostraca, and, in fact, is most commonly found regulation hatching and swimming in cold and cool waters. Without scientific studies of strictly cool- or Anostracans live in habitats with amazing ex- cold-water fairy shrimps to demonstrate how their tremes of alkalinity and dissolved salts. Com- metabolic rates and tolerance physiologies might bined, these are sometimes referred to as salinity, work differently, we are left out in the cold (so to but we will use the more appropriate term total speak) for an answer. Coincidentally, Branch- dissolved solids or TDS. Just as amazing is the inecta mackini and its notostracan relative, the fact that not all that much is known about how tadpole shrimp Lepidurus lemmoni, sometimes fairy shrimps accomplish the feat of dealing with occupy the same spring pools. If we were to use this fantastic spectrum of ionic materials (the dis- our research data from this cool-water tadpole solved charged particles which in total result in shrimp (Eriksen & Brown 1980c) as a suggestive the osmotic concentration of the medium: e.g., + + = = model for how a cool-water fairy shrimp works, Na , K , Ca^, CI , C03 , S04 ) and the influx or we would expect to see little tolerance in the latter efflux of water that occurs as a result. As a gen- of environmental conditions that exceed those at erality, think of the problem this way. All organ- which it demonstrates its maximum metabolic isms have a certain concentration of various ma- rate. In fact, once that magic temperature is sur- terials in their tissues and blood. If that level passed, metabolic rate would decline catastrophi- strays very much from a given norm, the beast is cally and the animal would soon die. in big trouble. You are probably quite aware of But back to survival in warm-water, low-oxy- that for yourself, given all the emphasis your gen habitats. As the last solution we can muster, doctor undoubtedly lays at the altar of blood tests. remember that a supplementary method of obtain- For an aquatic creature, like our fairy shrimp, ing and distributing 02 is available in the form of water is the medium in which it lives, and that hemoglobin; that is, hemoglobin binds far more medium moves into or out of its body depending 02 than could be dissolved in blood without it. upon whether environment or organism has more Hemoglobin-bound oxygen is picked up from the water per unit of volume. If water outside is relatively high 02 concentration at the body's "fresh" and thus contains little dissolved material, surface and released in the lower-oxygen envi- water will move into the body where there are ronments of tissues. Although hemoglobin has relatively more dissolved materials and therefore

17 Ch. 3. Ecology of fairy shrimps less water. If this process continues, our aquatic lation, this physiological ability requires several creature soon has a volume problem, and must steps, and a relatively impermeable body surface make its "bladder gladder" by urination. If the so that the natural tendency of water to move out surrounding briny medium contains more salts and salts to move in is considerably decreased and less water than an equivalent volume of (Croghan 1958b). First, Artemia drinks its salty blood, water will move out of the organism, thus milieu. Because the gut must be highly permeable dehydrating it. This natural and passive process to allow products of digestion to enter the hemo- of water moving from its higher to its lower con- lymph, salts from the water that it engulfed also centration, into or out of any living thing, is called enter. Second, because NaCl in the blood is osmosis. maintained at an elevated level over that in the To put all of this into the fairy shrimp's world, gut, active transport must be responsible for the imagine the different osmotic consequences of difference. Because tissues generally have not dwelling across the full range of anostracan habi- evolved a mechanism "...that can...transport water tats: arctic-alpine, temperate, and desert pools. against large osmotic gradients.", by actively tak- The former are typically environments with very ing up NaCl, the tendency for water to move os- little dissolved material of any kind. The fairy motically from Artemia''s tissues to its intestinal shrimp, on the other hand, is relatively loaded fluids is lowered to "...a level that the active with salts, and so water moves into its body, soon mechanisms for water uptake can overcome." presenting it with an excess. At the other ex- (Croghan 1958d). In this way, the animal gains treme, evaporative desert pools often contain water from a very salty environment that other- higher levels of dissolved chemicals than does the wise would passively dehydrate it. Third, and animal, water tends to move out, and dehydration lastly, because the increasing NaCl content of the is a danger. blood cannot long be tolerated, Artemia must ac- How do anostracans compensate for these tively transport the excess back into its surround- ranges of TDS and osmotic water movements? ings. It does this not at the gut surface but via With the aid of the 9 species that have been stud- specialized salt-secreting cells in the epidermis of ied in this way, four of which occur in California, the branchiae of the swimming appendages we make the following general remarks. In order (Croghan 1958c). to maintain blood at ionic and osmotic concentra- Some California fairy shrimps, like Branch- tions different from that of the environment, that inecta mackini, B. gigas, and B. campestris, are is, to transport substances in a direction opposite found in pools which vary widely, both geologi- to their normal passive movement, fairy shrimps cally and seasonally, in their dissolved salt con- (yea, all animals) must expend energy in a process centrations. When the environmental TDS is low, referred to as active transport. Artemia francis- individuals of these species maintain body fluids cana, which resides in California's most briny at a more or less constant osmotic level above that waters and "...can tolerate a wider salinity range of their pools (hyperosmotic regulation). Regu- than any other multicellular organism...." lation continues until the concentration outside (Browne 1993), relies on this process to maintain equals the concentration inside (iso-osmotic point). the concentration of salts in its blood at a level As salts in their pool water rise further, the ani- lower, often considerably lower, than that of the mals then osmoconform, that is they "mimic" the environment. Referred to as hypo-osmotic regu- TDS of the fluid in which they swim. However,

18 Ch. 3. Ecology of fairy shrimps once the dissolved materials in the blood increase one ion in the blood is increased to some level, to a point that is no longer physiologically toler- another may be increased or decreased to a differ- able, the animals perish. A greater tolerance of ent proportional concentration. Having said that, salt in body fluids explains why B. campestris can what do we know about the ion-regulatory ability be found in saltier environs than B. mackini, as of anostracans? Little! Six of the 8 species that well as why the latter may occur at times in more have been investigated in this way dwell in Cali- concentrated solutions than B. gigas (Brock fornia. Although ion regulation of K+, Ca^, 1988). California species have not cornered the Mg^, and CI" has been briefly studied, most work market on this mode of physiological adaptation. has dealt with Na+. For example, Home (1968) In the land down-under, Geddes (1973) noted demonstrated that Na+ was actively taken into the similar adaptations in two Australian species of body of Eubranchipus bundyi, even in waters very fairy shrimps. low in Na+, and concluded from this that the spe- Finally, there are anostracans that live under cies was well adapted to dilute habitats. the narrow constraints of water nearly as dilute as Branchinecta sandiegonensis and Streptocephalus the rain. For these moderate- to high-altitude woottoni, also inhabitants of dilute rain pools, species, the problem is to get and keep salts, and Branchinecta mackini which lives in much more to pump out the water that is constantly moving in concentrated alkaline waters, and B. lindahli osmotically. Although none of the California which dwells in both kinds of places, are de- species living in dilute environments have had scribed as being regulators of Na+ over certain their water and body-solute regulation studied, environmental ranges. In habitat concentrations several European fairy shrimps dwelling in simi- above and below their regulatory ranges, these lar habitats are known to maintain their blood at fairy shrimps are Na+ conformers until they perish an osmotic level higher than the medium in their (Gonzalez et al. 1996). These authors explain the pools, which is to say they are hyperosmotic different distributions of the three species by how regulators (e.g., Panikkar 1941; Ralph 1967). well they tolerate Na+ conformity at either end of These species have adapted differently from those their regulatory ability. For example, both B. just discussed in that they are able to regulate the sandiegonensis and S. woottoni sustain their blood concentration of their body fluids in waters of Na+ levels in the face of quite low habitat concen- much lower salt concentration ("soft" waters), but trations. However, following the cessation of die when the environment is saltier than them- regulation at higher environmental Na+ concen- selves because to osmoconform means death. trations, and as its level in the blood begins to rise Home (1968) believes that because all branchio- along with that of its pool, individuals begin to pods have blood osmotic concentrations much die; and so these species are restricted to waters of lower than other crustaceans (Potts & Parry rather low-Na+. Although B. mackini is able to 1964), thus a lower osmotic gradient between keep blood Na+ from increasing as rapidly as that body and environment, these creatures osmoregu- of its habitat, the animal is a poor hyperregulator late more easily in freshwater. Assuming this to of the ion. Absence of this species in low-Na+ be true, the ability would contribute significantly waters suggests that low levels in the blood are to the success of fairy shrimps in very dilute not tolerated; by contrast, comparatively high habitats. blood Na+ is endured as it conforms to elevated In the process of osmoregulation, animals dif- environmental concentrations, and so relatively + ferentially regulate ions. In other words, while high-Na waters are suitable habitat. Except for

19 Ch. 3. Ecology of fairy shrimps minor details, these same trends were mirrored by through the same surfaces by which it takes up two Australian Branchinella species for Na+, K+, oxygen. and Ca^ (Geddes 1973). Continuing with the Several times we have made mention of fairy Gonzalez et al. (1996) study, Branchinecta lin- shrimps pumping out excess water, yet we have dahli is viewed as a creature which reacts in the not identified the pumps. Adult anostracans pos- same way as B. sandiegonensis and Streptocepha- sess maxillary glands, so called because their lus woottoni in low-Na+ environments, and mir- ducts open at the base of these head appendages. rors B. mackini throughout the rest of the range Such glands are remnants of excretory organs, tested. You may not be too surprised to learn, analogous to kidneys, used by ancestors of crusta- then, that B. lindahli is found in pools similar to ceans. Apparently they play only a minor role in those occupied by the other three species. salt regulation of present-day fairy shrimps; how- When fairy shrimps typical of so-called "soft ever, the best guess is that they still' function as waters" regulate osmotically and ionically, where bilge pumps by dumping excess osmotically- do they obtain the needed salts? Remember that derived water (Croghan 1958d). brine shrimps spend energy in the process called active transport to counter the natural movement Reproduction of ions from the briny water in which they live to their lower body concentrations. Assuming active Those people who are gently touched by in- transport can function whether the normal os- tently observing fairy shrimp mating behavior motic direction be out of, or into, an organism, generally subdivide the process into a series of then such a mechanism, evolutionarily honed for actions (Belk 1991a) which could probably define soft-water anostracans, could account for move- their own. Such beautiful steps, so coldly enu- ment of salts from lesser amounts in the pool to merated, are: detection, orientation, station- greater levels in the animal. Panikkar (1941) taking, clasping, copulation, ejaculation, and dis- thought this to be true for the European fairy engagement (sigh!). Perhaps before discussing shrimp Chirocephalus diaphanus and further the intimate details of these activities, we must claimed that branchiae of the phyllopodia were admit that there have not been all that many sci- where this was accomplished. Add to the possi- entists who have studied such behavior. In fact, bility of active uptake of ions the fact that a modi- the generalizations of what goes on in the sex life cum of minerals is ingested in food, and we have of fairy shrimps come from only 10 of the more the best guess as to how our soft-water fairy than 260 species described world-wide (Belk & shrimp friends gain and regulate their salts. Brtek 1995). However, Belk (1991a) believes When you and I think of kidney function we these generalizations are reasonable "...given the tend to think of eliminating urine, a solution of morphological similarity of reproductive struc- mainly water and urea, the latter being a toxic tures in the Anostraca...." nitrogenous waste produced in the breakdown of Observers have noted that males seem always proteins. Although fairy shrimps may eliminate a on the prowl for mates, and while they have dem- small amount of urea in the water they pump out, onstrated detection of females by males involves about 75% of their nitrogenous waste is ammonia vision, nothing has been established concerning (Bernice 1972). Ammonia is a highly soluble gas the role of chemicals or water-borne vibrations as and rapidly diffuses away from the animal cues to males about possible mates. Were we

20 Ch. 3. Ecology of fairy shrimps

analyzing humans, a male who had detected a serratus; a few hours for Linderiella occidentalism female might next be seen to "make a pass" at his or days as seems to be the case in Artemia francis- prospect. By contrast, fairy shrimps are sorta dull. cana (whew!). Orientation merely involves swimming over to the During these swimming soirees, with the male vicinity of any promising object; but with station- in firm clasp of the female, he curves his body taking the activity becomes more intimate. The around her abdomen then attempts to insert one of male of most species moves in below the female his penes through her genital pore and into her (remember, fairy shrimps swim on their backs) ovisac. She will generally not allow his entrance and positions his head next to the dorsal surface of if already carrying fertilized eggs. However, her genital segments. Just to demonstrate not all when ripe eggs are present several struggling ef- fairy shrimps practice the same routine, males of forts may precede ultimate success. Not surpris- Streptocephalus and Thamnocephalus will place ingly, successful copulation, which lasts from only their heads just above the female's ventral brood a few seconds to several minutes, is very stimulat- pouch. However, from either position the result is ing to the male, and he soon ejaculates. For those the same. The male aligns his body with hers and so inclined, sperm can be watched flowing into follows her every scintillating move. the female's ovisac in slow-mating fairy shrimps Satisfied that this lovely creature is for him, like those of the genus Eubranchipus. Watched or the male quickly grabs the female from behind not, once the ejaculatory act is finished there with his antennae by placing them around her seems to be no biological sense for hanging body between her last pair of legs and the anterior around, and the pair soon disengages. In the in- end of her brood pouch. In typical female fashion, seminated female, "shutters", which separate the this lady fairy shrimp not uncommonly resists the ovisac from the lateral pouches where eggs have male's embrace by briskly thrashing about, an been stored, now open, allowing eggs to flood into activity which often results in her escape. This the ovisac, mix with the sperm, and be fertilized certainly illustrates that throughout the animal (Criel 1980). The male, as males are sometimes kingdom, including humans, not all males are prone to do, swims off to detect another female acceptable to every female at any moment, and whose delicately beating phyllopodia and entic- that females are involved in choosing a male ingly protruding brood pouch lure him to repeat rather than merely being overwhelmed by any one the sex-behavior sequence. Ah, those insatiable that happens by and demonstrates active interest. males. Although not all the cues used by fairy shrimps in If one were to try to draw meaning from choosing mates are known, evidence suggests variation seen in the reproductive process just species-specific antennal shape and ornamentation described, unsurprisingly, ecological realities are do aid the female in choice of a male (Belk 1984). probably at its root. For example, fairy shrimps Once the procedures for evaluating a prospec- typical of hot, short-lived, fast-drying pools might tive mate are complete, and the male in question be described as of the "wham, bam, thank you is found acceptable, clasping occurs, an activity ma'am" type. In pools with an intermediate lon- which may last only a few seconds in strepto- gevity, fairy shrimps are more deliberate as they cephalids, thamnocephalids, and the branchinec- proceed through the reproductive process. Fi- tid B. lindahli; several minutes in Eubranchipus nally, long-lived waters sport species which stay

21 Ch. 2. Biology of fairy shrimps in each other's embrace for an extended period of the sediment and allows them to float. Floating time; and why not, there is no need for hurry. not only makes them subject to passive dispersal within the pool (De Walsche et al. 1991), but also Development of cysts places them in higher concentrations necessary for the energetic hatching process. If the cyst Immediately after fertilization not only does walls of fairy shrimps function as do those of clam embryonic development begin, but the shell shrimps, and there is no reason to believe they do glands of the female secrete chemical substances not, then they also provide some physical protec- into the mix of seminal fluid and fertilized eggs. tion from abrading effects of soil particles being Then an amazing thing happens. This material moved by water or wind, as well as from lethal forms a thick, usually multilayered shell around effects of ultra-violet light (Belk 1970). each developing embryo. Talk about "better liv- Although we have commented on the amazing ing through chemistry"! By the way, this layering cross-sectional structuring of the wall of the cyst, is not at all analogous to dipping fish sticks in we would be remiss not to inform you that its batter then congealing it in place by frying. In- surface-sculpturing is just as amazing, and varied, stead, as the material solidifies different layers and often species specific! (See Fig. 3.2, p. 56). develop, some spongy, some solid (De Walsche et Richard Hill of the Environmental Office of Cal- al. 1991; Lee et al. 1994); and of course the elabo- Trans in Sacramento and Bill Shepard of Cal rate structural details developed in the various State University, Sacramento, are working on a species also vary wonderfully. What controls scanning electron microscope (SEM) photo- formation of architecturally different layers, the graphic catalog for cysts of all California species. variation within species, and the intricate differ- Watch for this one! But in the meantime, refer to ences among species, lies in the realm of the un- work by Mura (1991a, 1992b) where you can see known. most of the cysts of Branchinecta species from Adaptive significance of structural differences North America, and California's Thamnocephalus among shell layers has been the subject of some and several of its streptocephalids. The publica- conjecture. Structure is not just for structure's tions of Brendonck and Coomans (1994 a,b), sake, so the suggestions are based on the universal where cysts of Streptocephalus species of Africa relationship between the way something is built are displayed, give you a good idea of the variety and its function. With regard to the spongy layer, exhibited in this genus. its interstices are of course filled with fluid when Concurrent with shell development, embryonic formed in the ovisac; but when the cyst is depos- development, which also began immediately after ited and dries, the moisture is replaced by air. fertilization, proceeds apace for a day or two. The suggestion has been made that these spaces, During the process the embryo molts (sheds its like those in a down vest, offer thermal insulation exoskeleton) once or twice, adding the shed mem- to the cyst. Frankly, we find this supposed benefit brane^), the last of which is called the hatching difficult to imagine given the tiny size of cysts membrane, to the inelastic and protective shell, or (0.15-0.40 mm) and the long periods of time they tertiary envelope, surrounding it (Belk 1987). must withstand high or cold temperatures or both. When development reaches a late gastrula stage, A much better suggestion it seems to us is that further maturation stops, metabolism is drastically trapped air makes cysts buoyant when water re- slowed, and the embryo is isolated from the envi- turns, a condition which helps elevate them from ronment by a membranous barrier through which Ch. 3. Ecology of fairy shrimps

only gases and water freely pass (Drinkwater & Mono Lake), cyst production may be triggered Clegg 1991). So, the cyst, or "resting egg", is when the length of day becomes too short, while really a shelled embryo, analogous to the seed of a in temporary waters high salinity, low 02, and flowering plant, in a state of suspended develop- extremes of temperature are more likely the trig- ment referred to as diapause. gering factors. There is even evidence that indi- At this point the cysts of most species are vidual females of Artemia differ in their genetic ejected through the genital pore to fall to the pool tendency to reproduce more commonly one way or bottom, or, like the Titanic, the female carries the other (Lenz 1987; Lenz & Browne 1991). them to the bottom enmasse at the time of her When mature, cysts, like plant seeds, can death. In some cold-water species, however, de- withstand extreme environmental conditions. velopment takes a relatively long time with the Because of their protective coatings built of mate- result that some of the process occurs after the rials not affected by the enzymes pepsin, trypsin, cyst is dropped into the pool (Mossin 1986). If or lipase (Home 1966), they are not digested when the female survives for an extended period, she moved down the intestines of animals as long as will continue to move successive clutches of eggs they have not been punctured or smashed in the into her ovisac, each clutch being fertilized by a process. But it is when desiccated, and cysts are new mating, most likely with a new male. How- nearly free of moisture, that tolerance of real ex- ever, each batch of eggs undergoes development tremes begins (Clegg 1967). For example, they and ejection before the next clutch can be simi- can now be subjected to temperatures near boiling larly processed. In long-lived species like Strep- (Carlisle 1968), be frozen for months, even with- tocephalus sealii, Anderson (1984) estimated that stand near vacuum conditions for 10 years without a single female, living for three months, may pro- damage to the embryo (Clegg 1967). Of course duce more than 1,500 cysts. Wow! these are the abilities which allow anostracan Both the Mono Lake and San Francisco brine species to be distributed through alien environ- shrimps may alter the typical reproductive pattern ments and over great distances, as well as be just described. Their fertilized eggs can remain adapted to a life in basins which dry or freeze unshelled and continue development in the ovisac solid sometime over the course of a year. And until a larval stage is reached. Swimming young also as with plant seeds, cysts do not hatch until are thus expelled rather than cysts. For those who they receive proper environmental signals sug- like to add to their vocabulary, the latter repro- gesting appropriate conditions for the species to ductive process is said to be ovoviviparous, while successfully complete its life cycle. those with the more typical pattern are referred to In mountain snow-melt pools, the appropriate as oviparous. Females of Artemia switch between stimulus (perhaps cold, pure melt-water) presents the two depending on environmental conditions. itself unfailingly each spring, and cyst longevity And what are the environmental cues? Perhaps a need not be great. Having said that, no one knows favorable growing season, as indicated by suffi- what a cyst's life expectancy is for species living cient oxygen, and water at an appropriate tem- in predictable waters of this type. In the desert perature and salinity, stimulates larval release, regions of California, one of the necessary stimuli, whereas more stringent environmental conditions water, may not come for years on end. During trigger cyst development. such extended periods, cysts must also ride out In large, comparatively static systems (e.g., temperature extremes that humans might see as

23 Ch. 3. Ecology of fairy shrimps verging on the ridiculous. During the summer, at low temperature before the return of somewhat soil temperatures reach in excess of 65°C (150°F) warmer water in spring induces hatching (Lenz day after day. Carlisle (1968) even describes tem- 1980; Dana 1981). peratures of 80°C in the desiccated soils of Afri- In other anostracans, the return of water and can pool basins containing cysts of Streptocepha- any number of supplementary environmental lus and the tadpole shrimp Triops. During the stimuli, acting singly or in combo, are possible course of winter, cysts may be warmed daily, but stimulators of the hatching process. Among them, frozen each night. Still, under such conditions at temperature always exerts a fundamental control- least some of them survive 15 years, while others ling influence (Belk & Cole 1975). In at least two can probably make it more than 2-4 times that desert species, we know the rush of low-salinity long. We say this with some authority because water onto the dry, saline, playa lake bed where Clyde has stored dry soil samples from that won- cysts lie dormant triggers hatching (Brown & derful Montana "Cow Paddy Puddle #1" (Eriksen Carpelan 1971; Daborn 1975), and when dis- 1966), containing cysts of Streptocephalus sealii, solved materials increase to around 1,000 ppm, for 25 years, and had many successful hatches hatching ceases. Brock (1965) claimed that low when water was provided. By contrast, Clegg 02 is the hatching trigger for Eubranchipus bun- (1967) noted viability of Artemia cysts decreased dyi. However, Mossin (1986) convincingly re- with time to the extent that only a few released futed that notion by showing high C02 or low pH larvae after 15 years and none were viable at 28 is actually the stimulus for a related species, and years. Although it may be folklore, Clyde swears by arguing that sufficient oxygen must be avail- he has read somewhere that a reasonable percent- able to allow the energetically expensive hatching age of Artemia cysts hatched when doused with process to occur. While hatching takes place only water after sitting in a vial on a museum shelf for within a limited range of temperature (Belk about 100 years. Such a remembrance is given 1977a), and clearly not the same range for all credence by the report that exploratory oil drilling California species, those of us familiar with fairy near Utah's Great Salt Lake yielded buried Ar- shrimps readily admit that the real complex of temia franciscana cysts, carbon-dated at about environmental cues for hatching is unknown for 10,000 years old, a small number of which most species. hatched when placed in water (Browne 1993). No matter the state of our knowledge, once the True or not, ain't life amazing - and wonderful? appropriate environmental stimuli present them- selves, and only then, does dormancy end and Hatching development begin again. Byproducts from this reinitiation of metabolism accumulate around the Cysts are usually dried, frozen, or both before embryo, so water moves in osmotically and even more cues finally break dormancy and the stretches the flexible hatching membrane. The hatching sequence begins. An exception to this is resulting outward pressure breaks the inflexible the Mono Lake brine shrimp. Because Mono outer membrane, if present, and the shell. Further Lake is permanent, the opportunity for drying or expansion ruptures the hatching membrane and, freezing is small. Therefore, Artemia monica has voila, the embryo is freed to meet the dynamic developed a mechanism that makes environmental challenges of its aquatic world (Fig. 2.1, p. 25) sense - a long period of fall and winter incubation (Belk 1972, Rosowski et al. 1997).

24 Ch. 3. Ecology of fairy shrimps

Mossin's (1986) studies of a species of of appendages called the nauplius (Fig. 2.2, p. Eubranchipus revealed a variation on the timing 26). In some species a metanauplius appears, of this process that may be widespread among this being a slightly more developed stage in cold-water forms. Here, in late fall or early win- which the beginnings of thoracic phyllopods are ter, the embryo falls free of the shell but remains visible (Fig. 2.2, p. 26). Both types of larvae in a quiescent state (referred to as "prehatched") swim jerkily using their three pairs of functional in the small cocoon formed by the hatching mem- limbs. Although you certainly would not guess it brane. Finally, when ice melts in early spring, at this early stage, these appendages are really the additional environmental cues trigger activity, and fairy shrimp's two pairs of antennae and its man- the larva emerges into the larger volume of its dibles. Because growth is limited by the exoskele- pool. ton, the latter must be unzipped and cast off, that Given genetic variability among cysts, and the is, molted, for increase in size to occur. And so it microenvironment each occupies by chance in a is that at each molt these amazing creatures will pool basin, not all hatch at a given wetting. How- enlarge in length and girth as they add segments ever, those that release larvae do so within a lim- with their attendant appendages. The process ited time span - at most a few days. And with the continues from nauplius, through metanauplius hatch, the cycle of events that leads from desic- and juvenile, and into adulthood. Such gradual, cated, embryonated cysts, through tiny larval incremental growth contrasts starkly with the stages, to gracefully swimming adults is repeated metamorphic growth of butterflies whose form once again as it has since the early morning of changes drastically as they pass from egg to larva crustacean time. to pupa then adult. When hatching happens, out pops a one-eyed, We don't think further elaboration of anostra- egg-shaped young larval stage bearing three pairs can embryology is pertinent to our book, so we've

Fig. 2.1. Sequence of events in the hatching of a fairy-shrimp cyst.

25 Ch. 3. Ecology of fairy shrimps

Fig. 2.2. Larval stages of fairy shrimps: Nauplius larva (above) and metanauplius larva (below).

26 Ch. 3. Ecology of fairy shrimps

neglected it entirely. However, should develop- Lake, a playa in the western Mojave Desert once mental details "tickle your fancy", the studies by used by Marines for gunnery practice. In a bull- Weisz (1946, 1947) of Artemia, and that of Fryer dozed ditch filled with muddy water, my colleague (1983) using Branchinecta ferox, will supply John Moeur and I (Clyde) spotted brownish fairy enough material, both external and internal, to shrimps. Such a color is not uncommon in turbid satisfy most any appetite. waters, but it is not because the animals are dirty, We encourage you to reserve for yourself some nor is it due to the clay particles which fill their quiet time for inquiry over a minimum of three guts; what the environmental cause and physio- weeks, and watch the anostracan population in a logical source may be are unknown. In a bomb near-by rain pool. You will not only be richly crater nearby, the fairy shrimps, though beige in rewarded by seeing these changes occur before this water of lesser turbidity, possessed a reddish your very eyes, but you will be able to place these cast. Dipping into the next turbid-water crater, events in the real-life drama that is daily unfold- our net yielded reddish males and pinkish fe- ing in the microcosm of your special pool. males, probably a result of different amounts of Unfortunately for some of you, a rain-pool may hemoglobin in their blood. This was an interest- be inconveniently far removed from your urban ing find because we had never seen B. lindahli setting. Others may get the urge to observe and with hemoglobin. The last site, another bulldozed share these marvels of life with their kids at an trench with turbid water, produced females that ecologically inappropriate time of year (no rain). appeared dark bluish-green, but this time the Some may be barred from a pool because it har- pigment was deposited in tissues along the ovaries bors endangered species (see Chapter 6). Not to and in extremities of the appendages. And what worry, merely visit your local aquarium shop and about the males? Paint them beige, much like the there you can inexpensively, yea cheaply, pur- color of all shrimps from the initial site. chase "sea monkey eggs" (Artemia cysts) or Branchinecta lindahli is widely distributed adults. Should it be the cysts you bought, merely both within and without California, and is found follow some simple steps on the package, and in a wide range of turbidities and dissolved solids. watch the amazing developmental and reproduc- Its California color variations, which also include tive processes anywhere at any time. red-orange and apple-green, seem to have no ob- vious connection with these physical factors, for Color in turbid and clear conditions, high and low TDS, and cold or cool waters, the animals' most com- Fairy shrimps are graceful and gorgeous, but mon color is the signature milky gray-white of conspicuously colored? Only sometimes. Most most fairy shrimps. The blue pigmentation we are semi-transparent and a nondescript gray- noted might hinge on a diet high in fl-carotene, white. Of the variety of hues that may beautify for such a diet appears to result in blue ovaries in these animals, the sources of many are unidenti- Artemia (Hata & Hata 1969) and Thamnocephalus fied, and the environmental cues that stimulate platyurus (Maeda-Martinez et al. 1995b). We their production are largely enigmatic. But don't find this scenario unsatisfying, however, because let that interfere with your sharing our delight in water in all depressions was turbid and therefore the startling range of colors exhibited one spring must not have been oozing with phytoplankton, day by Branchinecta lindahli at Emerson Dry all of which possess fi-carotene. Besides, although

27 Ch. 2. Biology of fairy shrimps all water holes had filamentous algae (which also "...dark brown in color, tinged with deep green - contain the substance) tangled in the branches of typical coloration for forest pool shrimps." Envi- brush that ringed the surface water, algal fila- ronment certainly seems implicated, but what ments have only occasionally been reported habitat clue or clues caused the change in colora- amongst gut contents of fairy shrimps (Maynard tion of the next generation was not pursued. 1972; Belk & Ballantyne 1996), and only one pool Like Walter Moore, both of your authors have had individuals decorated with blue ovaries. reveled in the various colors of Streptocephalus While reviewing this manuscript, Robert Brown sealii. For example, in a Tennessee pool Clyde of CSU San Luis Obispo reminded us that described it as opalescent, while in a muddy cattle Branchinecta mackini also possesses a blue pig- watering-hole in Montana the animals were the ment in tissues of its oviducts and it too lives only same light-brown color as the fluid in which they in turbid waters. Whatever its cause, the blue swam even though the source of the water was a substance may be canthaxanthin-lipovitellin, a clear, grass-lined "reservoir" in which all indi- material identified from yolk platelets of Tany- viduals were apple-green. In California, S. sealii mastix stagnalis (Zagalsky & Gilchrist 1976). is restricted to the high Sierra and Siskyou Lastly, the cause of blue deposits in appendages Mountains and thus usually to clear, although remains unknown as well, but it has not been sometimes tea-colored, water. Animals in these connected with ft-carotene in the diet. populations are mostly a beautiful deep green- Still on the topic of Branchinecta, we recently blue, but, in Lassen National Park, Clyde collected heard from Marilyn Myers, a graduate student at light purple individuals in one pool and green U. C. Berkeley, who netted B. dissimilis from a ones in another. In these cases the pigments ap- pool in the White Mountains, the highest known peared to be dissolved in blood and, to the esthetic fairy shrimp site in North America (3,587 m). detriment of all who would wish to view them, This unique anostracan, at this unique elevation, disappeared upon preservation. What the pig- certainly possessed unique brood pouches because ments were we do not know. However, Peeters, et they "appeared phosphorescent to me, like they al. (1994) described a blue substance (artemo- had light glands", Marilyn wrote. Talk about a cyanin) in solution in the hemolymph of both Ar- "White Mountain high"! temia (where it was first described by Krissansen Streptocephalus sealii is the most widely dis- et al. 1984) and Streptocephalus proboscideus. tributed anostracan in North America. In most You might find it interesting that this blue pig- habitats it displays the "typical" gray-white color ment is a break-down product of hemoglobin. But of fairy shrimps with the addition that its cerco- if artemocyanin is truly the substance causing pods are orange-red, a color attributed to trans- California-dwelling S. sealii to be green-blue, canthaxanthin (Murugan et al. 1995). Walter then we wonder why there should be a need to Moore (1955), the Louisiana scientist who has synthesize hemoglobin in the normally high 02 studied S. sealii more than anyone, transferred a levels of the cool pools in which they occur? We dozen of his favorite beasts from a ditch habitat to also wonder why no one has reported at least some a forest pool unoccupied by fairy shrimps. The red individuals, or possibly some strange-colored pool soon dried and remained desiccated for over critters whose hemoglobin is mixed with the 6 months. When water returned, so did Walter. green-blue of artemocyanin? Yes, he found fairy shrimps, but rather than being Another Streptocephalus, the Riverside fairy gray-white like those he introduced, they were shrimp S. woottoni, deposits an orange pigment in Ch. 3. Ecology of fairy shrimps its cercopods and sometimes along the edges of its than would be possible in its absence. swimming appendages. Such a color pattern Thinking we "know it all" concerning red col- sounds suspiciously like that in Thamnocephalus oration may get us into trouble, however. For platyurus placed on a yeast and B-carotene diet example, several scientists, studying Artemia (Maeda-Martinez et al. 1995b). In a control, ecology in salterns (ponds where sea water is animals given only yeast (no carotenes) were evaporated to concentrate salts) along their Span- gray-white throughout. The authors suggested ish coastline, noticed that only certain individuals that since orange extremities are typical of most T. were "a red color". So what, you ask? Why platyurus collected in natural pools, the color is didn't they merely assume it was hemoglobin and "probably" due to algae in their diet. Sounds go about their research? We suspect they rea- simple, eat algae, turn your appendages orange. soned as follows. If a low-02 environment makes However, such an explanation skirts the issue of the synthesis of hemoglobin advantageous, essen- whether algae can grow in the muddy waters typi- tially all animals would possess the pigment, yet cal of most habitats of T. platyurus and S. woot- only some were pink or red. As it turned out, all toni. In several pools near San Diego, not only pink individuals were parasitized by the cyst stage the extremities, but the entire body of many fe- of a tapeworm. One finding deserves another, males of Streptocephalus woottoni appeared right? So analyses of body chemistry showed bright red-orange. All males were gray-white higher than normal lipids, probably related "...to with orange cercopods. The red-orange hue did carotenoid pigments conveying a red color...." not remind us of hemoglobin, but if it wasn't this (Amat et al. 1991). You might ask what the rela- material, or linked to dietary B-carotene (which tionship is between being parasitized, body color, we would expect to affect males similarly), then and lipid content? A reasonable hypothesis is that we have no idea of its cause. If it was due to he- parasitization leads to castration of the shrimp, moglobin, it might be because females remain in and thus loss of its reproductive hormones. A deeper, more oxygen-poor regions of a pool, a change in hormonal balance affects body chemis- characteristic behavior of females brooding fertil- try widely, and probably causes the increases in ized eggs (Belk 1991a), while males spend more lipids and carotenoids noted. Castration seems time in near-surface waters. not to affect health of the shrimp otherwise; it merely allows energy normally directed into egg The fact that low 02 stimulates production of hemoglobin, at least in some anostracans, is best and sperm production to be utilized in develop- demonstrated in brine shrimps. From the work of ment of the parasite(s). Red coloration makes the Barbara Gilchrist (1954), we know that in salini- animal conspicuous and thus probably more sus- ties less than about 3.5 times sea water (about ceptible to predation by birds - an advantage to 125,000 ppm), hemoglobin generally cannot be the completion of the parasite's life cycle. detected in the animals. However, at concentra- Robert Brown tells us of a similar situation he tions above that amount, animals become increas- noted with Branchinecta lindahli from the Soda ingly red. Remember, the greater the salinity of Lake area of San Luis Obispo County. In his case, water the less 02 it can hold. Therefore, Artemia when an unknown parasite filled the body cavity increases production of hemoglobin, females more with its cells, the fairy shrimp became white, than males, as environmental oxygen declines, making infected individuals quite conspicuous. and by so doing transports more 02 to the tissues Bob also theorizes that birds feeding in the pools

29 Ch. 3. Ecology of fairy shrimps select these animals because they are easily seen - stores are used over a period of a few days, the again a boon to the parasites. color gradually disappears. Lastly, Maeda- Finally, Linderiella occidentalism a small fairy Martinez et al. (1995b) commented that nauplii of shrimp typical of a number of California's grass- Thamnocephalus platyurus are "green-bluish". land pools, though light gray-white in body color, Denton (previously unpublished) observed that has red eyes, a sharp contrast to the dark black even embryos possess an array of colors. When he eyes of all other Anostraca. In nature, most ar- deshelled cysts to measure their contained em- thropods utilize black pigments to keep light from bryos, to his pleasure he found gold embryos in leaking between units of the compound eye, but cysts of E. serratus; rust, white, and purple ones why native populations of L. occidentalis swim in inside those of Streptocephalus mackini; and cysts the face of this physiological generalization is not containing blue-green embryos of T. platyurus and understood. Sarane Bowen and her compatriots at T. mexicanus. We know of no definitive informa- CSU San Francisco have been able to gaze into tion about the source of these colors. Ah, embry- the red, garnet, and white eyes of mutants onic Technicolor, but why? (produced by radiation treatments) of the normally Obviously many of the reasons for color varia- black-eyed Artemia franciscana (Bowen et al. tion in fairy shrimps are largely enigmatic. But, 1966). She and her co-workers determined that might this stimulate some of you to seek answers the various pigments were merely different to the myriad of mysteries associated with color? chemical states of a substance called ommo- For starters, how about determining the chemical chrome (Kiykomoto et al. 1969). nature of the pigments displayed? When that is You have undoubtedly noted that so far we done, perhaps other fascinated followers of fairy have spoken only about adult fairy shrimps. shrimps will ferret out the factors which signal an Working our way backwards in the life cycle, we animal to mix its cauldron of bodily chemicals in know of only three species in which larval color such a way that colors appear which benefit the has been recorded for posterity. Dexter and Fer- beast's survival in its ever-changing ecological guson (1943) reported brilliant salmon-colored world. In the meantime, many fans of fairy metanauplii of Eubranchipus serratus. Gilchrist shrimps, including your authors, will merely re- (1954) noted that the bright red color of newly main in awe of some of the absolutely gorgeous hatched Artemia nauplii is due to carotenoids in colors carried about in the bodies of these grace- their fat stores and not to hemoglobin. As those fully-swimming creatures.

30 Chapter 3

ECOLOGY OF FAIRY SHRIMPS

Introduction to community ecology ample, you may not know the trash collectors or the bankers, but you would be in a terrible fix As your mind's eye sweeps across the Cali- were they to take their services elsewhere. fornia landscape it "sees" the great variety of hu- The Great Law for the universe and its living man communities through which you have trav- things (Second Law of Thermodynamics), the law eled: from Alturas to Zzyzx, Red Bluff to Redondo that describes the constraints for everything, even Beach, and including Laytonville and Los Ange- the California Legislature, states that ultimately les. Ah, yes, how they vary: you remember their "there is no free lunch", that is to say everything vast differences in land area covered, in human costs something; for humans that might be para- numbers, cultural diversity, complexity of econ- phrased by saying that "using money, costs omy, and esthetics. Some were nestled peacefully money". But for a more precise meaning, one amidst the pines along a little-traveled mountain which includes planets, people, plant life, pools, road; others lay pastorally on the rolling grass- ...and fairy shrimps, it is better stated that "using lands buffeted by winds and threatened only by energy costs energy". In other words, all things afternoon thunderheads. Some were but an eye- require and use energy. Because that energy can- sore along a desert highway; unfortunately, too not be obtained or used with 100% efficiency, many were sandwiched and all but choked to living things are in an insidious, downward, and death by urban sprawl and the ugly litter of ex- competitive spiral for the remainder. cessive waste. And so it is with the communities Fortunately, one form of energy can be con- in which fairy shrimps dwell, for many are the verted to another, like solar energy into food by parallels should one want to pursue such anthro- plants or into electricity by humans, but, in accor- pological-anostracan comparisons. dance with the Second Law, when conversions As with humans in their cities, fairy shrimps occur some of the energy is changed to heat, and are often the most numerous "large" and, there- heat as we all know dissipates away from our fore, conspicuous animal inhabitants of their bodies, our homes, and our cars, never to be re- communities. "Most numerous" usually means captured. So, the nitty-gritty reality is that as our these creatures occupy the first consumer level in original energy supply is utilized, some is frittered food chains. Prudence suggests we explain these away, and obviously new supplies need to be bits of jargon involving community economics. In sought to replace both use and loss. The latter is a fairy shrimp communities, just as in your own, major cost of "doing business", a major controller there are a number of jobs or "functional roles" of the human economy. And so it is with the rest that when filled provide the "services" that allow of our universe, including our planet and its other the community to function. You may not interact living things, including the economy of the com- with all your neighbors, but ultimately you and munities in which fairy shrimps dwell. others depend on what they accomplish. For ex- Fortunately, for humans and anostracans, the

31 Ch. 3. Ecology of fairy shrimps sun is a continual source of light energy that can and in like manner other animals eat the animals be transformed to a type of energy useful to living that ate the plants so that they too may have en- things. Although it might strike at the ego of ergy to drive their processes, is of paramount im- some engineers, conversion of solar energy was portance to humans, and to fairy shrimps! If you mastered more than a few years before their time were to gather together all the threads that link by certain bacteria, then by lowly algae, and fi- the specific feeding requirements of all species in nally by land plants. By the process called photo- a pool-community, you would weave a particular synthesis, plants take the ecosystem's initial step pattern, yea structure, on the fabric of life that in converting solar energy into the chemical en- describes your particular fairy shrimp community. ergy of glucose; thus, they are referred to as pri- The relationships that have evolved among and mary producers. Plants then reconfigure glucose between living things, in which the energy of into various products to make their own structure some species is captured and processed by others (e.g., leaves and wood) and reproductive items adapted to do so, are what we call food chains (e.g., fruits and seeds). In so doing, plants set the and food webs. In nature, energy flow along limits for the amount of energy available in a these feeding interrelationships is the measure of community, for more cannot be used than is pro- the community's economy; and success is deter- duced or imported. mined by the efficiency of energy use, not by the Faced with an inability to convert solar energy fantasy of an ever-increasing GNP! to their use, many animals meet their energy Thus, because of constraints described by The needs by eating plants or plant parts which they Great Second Law, every creature gracing this are adapted to consume and digest. Such plant- earth is obviously concerned with continually eating animals (herbivores) are referred to as "putting food on the table". As it does, it interacts secondary producers or primary consumers. with, or relies on, many creatures that provide These plant-eating animals use energy to gain and other essentials which aid its, and its commu- process their food; therefore, they cannot possibly nity's, health and survival. possess as much energy as they ate, and certainly not as much as is contained in the community's The fairy shrimp's aquatic community plants. This means that either the herbivore num- bers are fewer, or their biological material, as If we were to visualize the community in measured by collective weight (biomass) or energy which a fairy shrimp lives, one where the ethnic (calories), is less than in the plants. and job diversity is great, just who are the partici- We also know that the animals we call carni- pants providing the essential services that we are vores make a living by eating other animals, not likely to encounter? Approaching this challenge plants. And if our previous argument is followed as an ecologist might, we would first look at to its logical conclusion, the carnivores in the creatures who harvest the energy of sunlight. community should number fewer, or at least col- WOW, these come in a fantastic variety of shapes, lectively contain less biomass or fewer calories, sizes, and life styles - just as do humans in their than the animals on which they fed. communities. No surprise here! The fact that plants provide all the initial fuel At their simplest, there are the single- or few- for a community's economy, and that certain ani- celled blue-green bacteria and algae that live a life mals eat those plants in order to gain their energy, dispersed in the water column. Biologists call

32 Ch. 3. Ecology of fairy shrimps these phytoplankton. There are also algae that cluded in this locomotor menagerie are those begin life attached to some stable surface such as which have one or several long whips to propel the pool's bottom, including rocks and logs, or it them in spiraling trajectories. These are the may be other plants, living or dead, or even ani- flagellates. No simple classification of the eating mals! The many creatures which share this way habits of these tiny creatures exists, for many ab- of life are collectively known as periphyton, and sorb dissolved organic materials while others eat they are a tasty, nutritious smorgasbord for ani- organic particles, and thus are "animals". A mals adapted to eat from this table. number of flagellates possess chlorophyll, and, Algae are among the most ancient and ana- being plant-like in this way, are included in the tomically simple life-forms on earth; but in the phytoplankton as primary producers. Our tidy evolutionary scheme of things some ancestors of minds demand simplistic cataloging of commu- these aquatic organisms gave rise to more com- nity members; real life continually reminds us that plex terrestrial plants, adapted structurally, to this end we fool ourselves! physiologically, and reproductively to a life out of Not much larger than protozoans, but many- water. Inevitably, like many animals (most nota- celled in structure, are the Norelco shavers of the bly insects), some plants reinvaded their watery animal world. These microscopic creatures, origins. The ones who most commonly did so usually with two rings of beating cilia at their were the flowering plants, members of the com- head end that not only propel them through the munity that make most of the "tenement houses" water but sweep bacterial and algal food to their that root in the bottom of a pool and reach for its mouths, are called rotifers, or wheel animals. surface, sometimes piercing it. These flowering Although fairy shrimps need not concern them- plants, from pond-weeds to rushes, create the selves about collisions with such small-sized traf- structural complexity which provides the special fic, a different story might present itself with other habitats needed by many of the pool creatures. pond creatures. The most common constantly These are also the plants that are responsible for swimming animals other than fairy shrimps are the late-season edge-bloom which defines, and the water fleas (Cladocera; Fig. 1.1, p. xiv) and colorfully graces, California Vernal Pools. copepods (Copepoda). By comparison to adult In their communities, humans watch birds, anostracans, these creatures also are small usually pigeons and house sparrows, circling the (usually 1-2 mm). However, by virtue of their atmosphere between the tenements. In a pool, the sheer numbers, the pool may seem like Times aquatic "atmosphere" is filled with a much more Square on New Year's eve to a fairy shrimp. culturally diverse and therefore pleasing variety of Where the rub (pardon the pun) arises is most living things. Other than the countless numbers copepods, water fleas, and fairy shrimps are filter- of bacteria and the phytoplankton already de- feeders, that is, they filter small particles, includ- scribed, the midgets on the block include Proto- ing bacteria, protozoa, rotifers, and phytoplank- zoa, or single-celled animals. They teem in great ton, from the water through which they swim. abundance, occupying all levels of the consumer Similar feeding habits suggest competition for food chain. Ciliates, protozoans which possess a available "goodies", and so it may be. However, great profusion of cell membrane outgrowth as with the human business world, specialists of which beat to cause rapid movement, are the all kinds abound which stake out and capture a speedsters of the microscopic world. Also in- sufficient piece of the economy. By possessing

33 Ch. 3. Ecology of fairy shrimps different-sized filters, or feeding in disparate areas porary waters and, as you might expect given their of the pool, filter-feeders can specialize in only fantastic variety in terrestrial habitats, have spe- certain segments of the total resource and thus cialized along a number of aquatic life styles too. either minimize competition or out-compete gen- You will see snorkelers, aqua-lungers, and gill- eralists attempting to benefit from the same re- breathers, and if such adaptations get the best of source. Other small and constantly swimming your curiosity, check out the chapter on Respira- community members include some wonderfully tion (Eriksen et al. 1996) in Aquatic Insects of colored flatworms (Rhabdocoela), most of which North America. Although many of these insects probably use filter- and suction-feeding, and the are small, several of the larger, highly mobile spidery water mites (Hydracarina) adapted for ones are notable predators on fairy shrimps and sucking the body fluids of small crustaceans and other pool life. Of these, the predaceous water insects. beetles and their larvae (Family Dytiscidae) and a Larger members of the community just might true bug called a backswimmer (Family Notonec- include some fascinating close relatives of fairy tidae) are the most common. The majority of the shrimps spoken about earlier. The clam shrimps, other pool insects live on or near a submerged or Conchostraca (Fig. 1.1, p. xiv), often lie on the surface, using the latter for resting, protection, bottom, but as unlikely as it sounds they also and a place from which to launch a feeding foray. spend a good deal of time swimming...and filter- Such creatures include dragonfly larvae and their feeding. And, if you are wary of the statement relatives the damselflies (Order Odonata), both of that "truth is stranger than fiction", you might which can, and do, chow down on fairy shrimps. change your mind when you encounter tadpole Most of the other creatures which circumnavi- shrimps (Order Notostraca; Fig. 1.1, p. xiv) with gate the pool have little direct interest in fairy rhythmically-beating hemoglobin-filled phyllo- shrimps. They make a living either by grazing on podia. These creatures, some upwards of 70 mm plants, or by scooping up dead remains enriched long, and feeders on bottom debris and predators by a bacterial and fungal coating - a material you on fairy shrimps when occurring together, look might call "gunk" but which ecologists refer to as like something out of earth's fossil past. In fact, detritus. Such creatures are called detritivores they have changed little from their own fossils, and include mayflies (Order Ephemeroptera), and, given their large, flattened shield and caddisflies (Order Trichoptera), seed shrimps swimming legs, superficially resemble a fossil (Order Ostracoda), and scuds or sideswimmers group of early arthropods, a resemblance that led (Order Amphipoda). Also undertaking this way to a fishery biologist's embarrassing misidentifi- of life is a bug called the water boatman (Family cation. When accompanying an L. A. Times re- Corixidae), a beetle called the water scavenger porter to a desert lake to explain what life had (Family Hydrophilidae), and pond snails called burst forth following a rare summer rain, he "pond snails" (Class Gastropoda). As if this me- gasped when he saw tadpole shrimps and ex- nagerie of creatures is not enough with which to claimed: "My god, Trilobites! Trilobites haven't rub shoulders or cause traffic congestion, stand been seen on earth for 250 million years". So, go back for the "18-wheelers" of the pool. Although look in your pool. Who knows what you will tadpoles of most frogs are herbivores, adults are find. predators, and salamanders and their larvae, long Insects are common in some longer-lived tem- and lanky vertebrates, and also fairy shrimp

34 Ch. 3. Ecology of fairy shrimps

predators, are big enough to run down and eat plants. Finally, there are countless creatures almost everything else on the "highways" of the which eat dead stuff - dead plant or animal mate- pool. rial, dead of this year or last year, dead of what Fewer, but unfortunate for pool animals, are was produced in this pool or what was dropped or the voracious wading and diving birds that come blown into it from afar. Nothing goes to waste in and go. Now we can understand the use of the nature. Everything is sought and consumed by broad and filtering bill of the Northern shoveler someone. Here is the true meaning of "recycling" (duck) for collecting fairy shrimps. At an earlier which, if the organisms are left to do "their and much more naive time of life, your senior thing", forms raw products that allow production author thought the long tubular bill of a wading to continue. Here is the dynamic equilibrium of American avocet was obviously adapted for prob- nature in action! ing mud flats, not for "filtering" anostracans from Some pools, like small human resource-based a pool's water column! Dare I admit I had a nar- communities, are probably not so grand or com- row view of the avocet's world? While "doing plex as just described. Several are the reasons. science" at many a fairy shrimp's home, I have As physical or chemical conditions become severe watched in amazement as avocets waved their and cast a shroud of extremes to which only a few beaks back and forth in the water and grabbed species are adapted, food webs become much whatever they hit. What they hit was most likely simplified. One of the most striking examples is a fairy shrimp, but was also possibly something the salty and oftentimes warm waters in which which ate a fairy shrimp. Ah, the ingenuity of brine shrimps like Artemia franciscana and A. life, and the beauty and symmetry of a pool's en- monica flourish. Bacteria, an algal producer or ergy flow! two, the brine shrimps that filter these kinds of Fortunately for anostracans, circumstance tid-bits from the water, and a detritivorous brine rarely brings them together with fish. The fly may be about the only cast of characters pres- ephemeral nature of fairy shrimp habitat obviously ent. precludes fish in most cases. However, should Should you wonder if things can get even flooding link permanent and temporary waters, as simpler, then consider Rabbit Dry Lake, an alka- occasionally it does, and allow fish to enter the line playa in the Mojave Desert. Here during dry grocery store of a pool (e.g., McCarraher 1959; times we see a hard, flat, expanse of clay shim- Pereira & Gonzalez 1994), they will find fine mering in the summer heat. But when a storm cuisine that has no protection but numbers, time, dumps its contents on the encompassing moun- and the forest of pool vegetation in which to "get tains, soil- and organic debris-laden water rushes lost". Obviously this situation is not on-going, for hellbent to the playa below to fill it with water so the fish must find their way back to permanent muddy it looks like a chocolate milk shake; water water, or they too will be lost, in this case to the so muddy that light does not penetrate and photo- finality of drought for which most of the pool synthesis cannot occur. Surprisingly to some, species are adapted, but fish are not. Branchinecta mackini hatches and thrives in What a complex community it can be! There enormous numbers. Such a prolific event makes are the producers (plants), and those animals that it understandable why its major predator, Bran- make a living eating plants, or eating those that chinecta gigas, may be present as well, albeit in ate plants, or eating those that ate those that ate expected smaller numbers, say one B. gigas to

35 Ch. 3. Ecology of fairy shrimps

40,000 B. mackini. Other than the ubiquitous better; but if so, it would have a competitive ad- bacteria, that's the cast of characters, friends! No vantage, reproduce more, and ultimately predomi- other visible critters. But, you ask, "if there are so nate to the exclusion of the others. Species which many alkaline fairy shrimps, what serves as their are most likely to compete so intimately are those food?" We will provide an answer shortly in the which are structurally and behaviorally most section "What do fairy shrimps eat?" closely related. Most pools, puddles, and playas probably lie Given such sage words, one might not expect somewhere between the extremes described. And several kinds of fairy shrimps, particularly those should you follow the creatures in your favorite within a genus (e.g., Branchinecta), to compete water-filled micro-universe, you will certainly see equally and thus coexist while occupying what the comings and goings, searching and eating, generally appears to be the same niche. However, reproduction and decay, that all add up to the although finding different kinds of fairy shrimps particular economics of the community. in the same pool is not a rarity, it is atypical, es- FASCINATING! pecially in cold-water habitats (Eng et al. 1990; As intrigued as you may be in your own Graham 1995; Maeda-Martinez et al. 1997). To "personal pool", we ask that you be of broad per- our knowledge, three species is the record for spective. Do not get caught up in the simplistic California, while 6, collected in North Africa by mind-set of some poets, perturbed people, and Thiery (1991), is the world mark. So much for politicians who believe, at least state, that "if dogma! Or is it??? you've seen one, you've seen 'em all", for nothing In order to begin our discussion of the intrigu- could be further from reality when dealing with ing problem of coexistence of species, "Return temporary waters. To prove that point to yourself with us now to those thrilling days of yesteryear consider reading Balco and Ebert (1984) and Syr- when out of..." Laurasia came the thundering dahl (1993). They show, by comparing many phyllopod beats of the great Eubranchipus ances- features, that each pool is not only different, but tor (Belk 1995), and probably the other ancestral usually uniquely so, even from its neighbor. Not anostracans of most of today's North American only does the cast of actors change through the fairy shrimps (e.g., Branchinecta, Linderiella, pool's duration, but the timing of those changes Streptocephalus). When it was that founding may also be strikingly varied! populations arrived to settle pools in what we now call California is not known. What we do know is Coexistence of species of fairy shrimps that some 10-15 million years ago California's earliest recorded fairy shrimp, a species of Bran- In the previous section, we intentionally said chinecta, plied the waters of an alkaline playa in a little about different types of anostracans co- savanna or possibly basin-and-range setting near existing. Dogma has it that were two or more where Barstow (San Bernardino County) sprawls species to occupy "the same niche" (have exactly today (Belk & Schram in prep.). the same requirements and do exactly the same Under similar climatic conditions, whether 15 thing) they could not co-exist. The rationale is million years ago or now, even closely-spaced that, since by definition they are recognizably pools often vary considerably as habitats; so, different, one of the species must be able to "do its whenever founding populations arrived, natural thing" somewhat better, possibly only slightly selection immediately began the relentless process

36 Ch. 3. Ecology of fairy shrimps of selecting among different combinations of ac- discussed in the section in Chapter 4 "How fairy cumulating genetic variability at each site, thus shrimps got where they've got". In that context, it initiating the continuous procedure of honing each seems some species may get around more easily population to its specific conditions. than others (e.g., Branchinecta mackini, B. lin- Whatever the range of conditions was that dahli), given their flexible physiologies and wide prevailed around Barstow or throughout the rest distributions, in both North America and Califor- of California so long ago, the land forms and cli- nia. In Australia, Williams and Busby (1991) mate were not what they are today. The Sierra at note a similar broad occurrence of the tadpole that time was perhaps 1,000 m high, and volca- shrimp Triops australiensis. But as admitted by noes spewed their contents across the landscape, these Aussies, and as is true of our two species of particularly over the northern half of the range Branchinecta, no one has looked at their micro- (Hill 1975). Narrow, shallow seas extended anatomy with scanning electron microscopy, or across the Central Coast Mountains in places and protein dissimilarity as evaluated by electropho- into the Central Valley. In what is now southern resis, to determine if differences among popula- California, the South Coast Mountain Ranges, tions exist or are developing. Using such tech- although still low, had begun to rise from the hills niques, people are accumulating evidence suggest- that preceded them (Oakeshott 1971), undoubtedly ing that dispersal is not successfully accomplished creating ever-increasing aridity across the lands to as often as might be imagined or thought (Belk & the east. Cole 1975; Dumont et al. 1991; Fugate 1992). Now superimpose upon these circumstances Still, should chance introductions occur, considerable change in the geological landscape transplants and residents may be different enough that began in the neighborhood of 10 million that they utilize separate fractions of the resources years ago. The Sierra began to rise, and the South in a structurally simple puddle; or they may re- Coast Mountain Ranges continued their progres- main "isolated" from each other by occupying sive uplift, blocking further the movement of rain- unutilized or under-utilized portions of a large, bearing clouds to the east. Knowing this, we can structurally complex pool (Hamer & Appleton begin to appreciate the increasing topographical 1991; Thiery 1991). To appreciate the fact that and climatic isolation of pools, as well as Cali- pools can truly be structurally complex, you may fornia's increasing isolation from much of the rest have to change your impression that an ephemeral of North America. Of course the general drying water-body is merely a simple dimple full of wa- and warming trend since Pleistocene times about ter. Although such a view might approach reality 10,000 years ago has further added to the increas- in tiny potholes, puddles, and wind-swept turbid ing hindrance of gene flow between pools. And so playas, deeper, longer-lasting habitats, particu- fell the fickle finger of fate that gave us this labo- larly those containing areas of rooted vegetation, ratory called California, which not only offers often provide great structural and thermal com- genetically differing populations of the same spe- plexity. Hearken back to our discussion of "The cies in different pools, but the evolution of a myr- fairy shrimp's aquatic community" (pp. 32-36) for iad of different species, including its great number a description of such a place. of endemic organisms, among which are some of With regards to coexistence of species, or lack its fairy shrimps. of same, competition which excludes a species is Isolation of California is not complete, of most likely when the environment is predictable course, because of several methods for dispersal and the competitive advantage is expressed gen-

37 Ch. 3. Ecology of fairy shrimps eration after generation. Should habitat condi- one type of fairy shrimp may be stressed and see tions change slightly, or considerably, the advan- its population decline while another finds condi- tage may be shifted from one type of anostracan to tions much to its physiological liking and "comes another. Temporary rain-pools and the environ- on like gangbusters". In other words, although ments in which they form are normally the quin- two anostracan species may be found together tessential example of habitat capriciousness. Im- occasionally, there should be significant differ- portant environmental factors can vary, often ences buried somewhere in their biology that ac- significantly, from year to year, and of course count for their coexistence. Ah, for inquiring through the seasons of any given year (Dexter minds to dig in and ferret them out! 1967). These include temperature, time(s) of pool So, having explained some of the possibilities filling, if they fill at all, and how long they hold for coexistence of species, we must admit there is water. Thus, in absence of a predictable environ- really nothing important known about the degree ment that gives a competitive advantage to a par- of competition among coexisting fairy shrimps. ticular species, a disturbance-based "dynamic In most biological systems competition is difficult equilibrium" is established between two or more to demonstrate, and no experimental work has forms, shifting the competitive advantage back been undertaken with anostracans. When coexist- and forth, and, as a consequence, allowing coexis- ing species show differences in structure, behav- tence over time. Under these circumstances, ior, and ecology, we should probably best begin competitive displacement (exclusion) occurs in- with the assumption that these are expressions of frequently (Huston 1994). genetic selection which minimize competition If some level of competition does exist, then between closely related species. However, not what are the structural and behavioral differences much is known about such differences among that explain its minimization among similar fairy fairy shrimps. For example, we are aware of only shrimp species, you may ask? Perhaps these fil- 6 measurements of filter size (Fiyer 1983; Mer- ter-feeders have evolved dissimilar filter size, al- tens et al. 1991; Schrehardt 1987; Helm 1998), lowing one species to utilize a different size-range and four are for species not even found in the of food particles from the total food resource than U.S., let alone California. What we know about does another. That animals in different life stages anostracan physiology, tolerances of temperature have different sizes of filters, and therefore feed and salt included, is also fragmentary. Observa- on different foods, seems intuitive. Perhaps dif- tions concerning behavioral differences are min- ferent behavioral feeding strategies have come uscule in number, and reports concerning what about so that one species feeds more on or near life-cycle stages were present with coexisting the bottom while another feeds higher in the water species are fewer than that. column. In other cases, temperatures at which So much for refined theory, informed guesses, cysts hatch may separate species by season, or if and what we do not know. What can we tell you they hatch at the same time, perhaps because of about the coexistence of species of fairy shrimps? different rates of development, young of one spe- Well, we can note which ones have been found cies do not mature until adults of another are on together (Table 3.1, p. 45), and we can cite several their last leg (or perhaps we should say phyllopo- known examples that may explain how fairy dium). As the season progresses, and evaporation shrimps could coexist in California's ecological of pool water leads to increased salt concentration, settings.

38 Ch. 3. Ecology of fairy shrimps

We begin with the association of Branchinecta while the tips of the "scraper's" phyllopodia are gigas (a predator reaching 150 mm in length) and armored with spines adapting it for this additional B. mackini (its prey, about 30 mm long). These activity. species obviously share physiological similarities Also interested in limb structure and feeding that allow them to live in the same alkaline pools, differences, Graham Daborn (1979), a Canadian in the same life stages, at essentially the same scientist, compared phyllopodia of a number of time. However, the predator has evolved gargan- genera and species. Included among them were tuan size, the greatest length and bulk by far of three that occur in California, two of which may any fairy shrimp species, has its adult appendages co-occur (Branchinecta mackini and B. lindahli) modified for capture of large prey rather than for and one of which (B. lindahli ) has been found at filter-feeding, and has evolved the behavioral one time or another with 7 other California anos- patterns necessary to catch B. mackini for its food. tracans. He noted that both B. mackini and B. B. gigas has also been infrequently recorded coex- lindahli, which attentive eyes have seen scraping isting with B. lindahli, so its feeding behavior at times (Daborn 1977; Tasch 1970; Eriksen, & appears satisfactory should the latter be the sig- Belk pers. obs.), also have spines along the outer nificant food item in its habitat. Although the edges of their appendages. Well, all do except B. main food supply of B. gigas certainly consists of lindahli females which possess fine setae instead. anostracans, hors d'oeuvres include various spe- Could it be that not only are species separated by cies of copepods which it devours as it swims such behavioral and structural differences, but through the turbid waters of its home (Anderson also that males and females of some species 1970; Daborn 1975). minimize feeding competition in this manner as Differences in feeding strategy, involving be- well? Ah, more questions! havior and structure of appendages, have been Before we run to the field or lab to look closely cited (Modlin 1982) as the reason that two species at our less-observed species, know that Bran- of Eubranchipus coexist in the central and eastern chinecta longiantenna may be a scraper as well, United States. Because so little is known about for some of our old drawings show the outer edges California's species of Eubranchipus, a similar of its appendages adorned with spines (Fig. 3.1, p. comparison cannot be made here. Yet the general 47). If this be the case, then some other mechan- differences in feeding behavior described in Mod- ism must minimize competition between B. lin- lin's paper have been recorded for a number of dahli and B. longiantenna when they occur to- other species, including some in California, so gether, as in the area around Soda Lake in San they warrant mention. As we know, fairy shrimps Luis Obispo County. By contrast, Artemia fran- are said to be filter-feeders, but not all are just ciscana is probably a pure filter-feeder, for the "pure filter-feeders". Using Modlin's example, outer edges of its appendages possess only long although Eubranchipus holmani remained in the setae (Daborn 1979). water column sifting out what living and dead Having just mentioned Soda Lake, let us tell "particles" it encountered, E. neglectus (mis- you that this is a very salty place and Artemia identified as E. vernalis) added to this repertoire therefore relishes the place. In late April of 1991, by occasionally scraping the bottom with its Larry Serpa, a regional manager for The Nature phyllopodia and thus collecting a load of detritus. Conservancy, collected not only A. franciscana Modlin noted that the tips of appendages of the from Soda Lake but, for the first time and still the pure filter-feeder are edged by many fine setae, only time in California, Branchinecta campestris

39 Ch. 3. Ecology of fairy shrimps as well. Larry did not obtain data on the popula- when S. woottoni attains sufficient size to be col- tion structure of these two species, but our best lected in a normal dip net. However, by the time guess is the population of B. campestris was de- most individuals of the latter species are mature, clining while that of A. franciscana was begin- B. lindahli has disappeared, and temperatures no ning to boom. We say this because that is what longer drop low enough to stimulate another of its Broch (1969) found in his study of populations of hatches. Why this beast has taken leave when these two species in four lakes in the state of adults can probably tolerate the water tempera- Washington. Broch felt the reasons for his obser- tures, and almost certainly the water chemistry, is vations were rooted in the different biologies of not understood. What we do know about its lon- the species. For example, in Washington, Bran- gevity suggests that age might be the reason. chinecta campestris begins to hatch early in the Yep, senile fairy shrimps; and more opportunity season when water temperatures approximate 4°C for research! and salinities are low because of snow-melt and Although the previous story seems straight- runoff. Although Artemia can hatch in distilled forward enough, life in the co-occurrence lane water, it needs temperatures in excess of 10°C to isn't necessarily all that simple. Consider that the stimulate the process. Because B. campestris situation just described occurs in western River- cannot regulate hypo-osmotically, it is limited to side County. Yet, but a few miles away on the the habitat's "low-salinity" phase. By contrast, southern coastal mesas of neighboring San Diego the hypo-osmotic regulatory ability of A. francis- County, the preponderant resident anostracan is cana allows it to live on in the grandiose quanti- Branchinecta sandiegonensis (Simovich & Fugate ties of salt that accumulate when wind mixes 1992; Fugate 1993). Of the many pools on the fresher surface water with deeper saltier water, southern mesas, in only three deeper ones on the and when evaporation concentrates salts in the Miramar and Otay mesas have B. sandiegonensis later life of the pool. and Streptocephalus woottoni been recorded to- Physiological separation of stages in the life gether; by contrast, on the coastal mesas in north- cycle is also important when Streptocephalus ern San Diego County, where B. sandiegonensis is woottoni, the endangered Riverside fairy shrimp, much less common than B. lindahli, the former co-occurs with Branchinecta lindahli. Here is a has been collected with S. woottoni but twice, the "togetherness" apparently allowed by differences latter a number of times. Furthermore, given that between the species in duration of development the distributions of the two branchinectids over- (Hathaway & Simovich 1996). What this all lap, we find it intriguing that on only three occa- means is that B. lindahli hatches well, and in sev- sions, and only in degraded puddles, have they eral days, from 5-15° and poorly at 20°C as dem- been found together (Simovich & Fugate 1992; onstrated by Denton's work (Belk 1977a), then Moeur pers. comm.). We would not argue too develops rapidly (1-3 weeks) to maturity. S. heartily with the individual who feels this situa- woottoni readily hatches between 10-20°C, with tion smacks of competitive exclusion, but for the some larvae even appearing at 25°C, but the proc- real answer, it's time for some experiments. ess takes 1-2 weeks. Development is slow as By way of introducing you to the secretive es- well, with maturity requiring 7-8 weeks. Thus, capades of another fairy shrimp endemic to Cali- during the cool-water stages of a pool in winter, fornia, we note that collections from the largest B. lindahli is the conspicuous resident, and it is habitat of Streptocephalus woottoni and still holding forth in late February or early March Branchinecta lindahli, a valley grassland pool in 40 Ch. 2. Biology of fairy shrimps

Riverside County called Skunk Hollow, have eriellas, the fact they are different genera means never yielded a third anostracan in the flesh. Yet, they possess sufficient structural and behavioral hatched in the laboratory from cysts in its mud is differences to allow co-existence. Maybe. a third species, Branchinecta lynchi. This crea- Whatever the case with Linderiella, the situa- ture is widely distributed throughout the grass- tion with Branchinecta conservatio remains un- lands of California but is seldom abundant any- explained. So, into the void steps Brent Helm, where (also a situation not understood), particu- who informed us recently that he believes he larly where it co-occurs with other species. Al- knows why B. lynchi cannot tolerate this though no published studies deal with specifics of branchinectid. First, both species hatch when its life history, Helm (1998) determined that it cold water fills their pool basins. Second, B. con- hatches, like B. lindahli, at cool temperatures. servatio produces but one cohort of numerous Why then has it not been seen swimming in individuals per year, while B. lynchi may muster Skunk Hollow? We can only guess. And our several, each with many fewer individuals. Last, guess is that B. lynchi was present but, true to B. conservatio is "hyperactive" and consequently form, in such small numbers that it just happened sets an amazing swimming and filter-feeding never to be taken in reported collections; or per- pace. On face value these similarities and differ- haps sampling was not done early enough in the ences may seem unimportant for the sparse indi- season to record its presence. Coexistence with viduals of B. lynchi. And in reality they may not adult S. woottoni, if it occurs at all, must be fleet- be very important, at least when both species ing, because the latter does not mature until wa- hatch and grow together in winter pools that last ters warm, usually in spring, by which time B. 6-7 weeks - a period of time in which each can lynchi has probably come and gone. How B. produce but one clutch of cysts. However, Brent lynchi gets on with B. lindahli is unknown, but it feels that if the two species were plunked together may be too similar in some way to the better- in longer-lived pools (the typical habitat for B. adapted B. lindahli to compete well, yet different conservatio), then, were B. lynchi to launch a enough to "hang in there" in a large, compara- second cohort, those nauplii would be eaten out of tively complex habitat like Skunk Hollow. We existence by the hyperactive filter-feeding activi- suggest this because in situations where pool size ties of the numerous B. conservatio. Great hy- is recorded, the smaller and simpler basins hous- pothesis, eh?! How about someone stepping up to ing B. lindahli have not yielded B. lynchi. test it? If someone does, they might begin with The wide distribution of Branchinecta lynchi the observation that the only time these two spe- generally includes the ranges of California's two cies have been observed together was early in species of Linderiella and that of B. conservatio, 1994 in two pools on the San Luis National fairy shrimps which also seem to require deeper Wildlife Refuge Complex in western Merced and larger pools. B. lynchi co-occurs with one or County. Most of the Refuge pools did not fill the other of the linderiellas with some frequency, until February of that year, and were low or dry by but only twice has it been seen on stage with B. mid-March. This period is long enough for both conservatio. However, in all situations where species to reproduce, but so short as to disallow a these associations were noted, B. lynchi was far second cohort for B. lynchi. Perhaps this is a outnumbered. Why? Maybe pond complexity is typical period of pool longevity here in the arid involved here too (although no such comparisons western edge of the Central Valley; if so, it might have been made); and maybe, at least for the lind- prevent B. lynchi from being "eaten out of exis- Ch. 3. Ecology of fairy shrimps tence" and thus allow co-occurrence. kali fairy shrimp, lives in a wide array of alkaline Finding Branchinecta lynchi with the midval- waters. Strikingly, if one were to consider infor- ley fairy shrimp (Branchinecta sp.) should not mation recorded from out of state, B. lindahli, the raise eyebrows since both can reproduce rapidly versatile fairy shrimp, is in fact more versatile. It and thus live in short-duration pools. However, is known from an even wider range of alkalinity, because they appear to have similar preferred beginning in the nearly pure waters of the quartz- homes, one might expect B. lynchi to have been monzonite dome pools that Clyde studied at spotted with our midvalley acquaintance more Joshua Tree National Monument, and extending than the three times so far recorded. Given their to such a seemingly trying habitat as an "alkali close taxonomic relationship, the reason may lie soup" the color of "black ink" in Nebraska in some form of competition so far unraveled. (McCarraher 1970). Nothing approaching the Branchinecta lynchi's quite unexpected one- latter conditions has been stumbled upon in Cali- known stand with B. mackini occurred in a road- fornia. side swale pool where the rather different ranges We read in Gonzalez et al. (1996) that B. lin- of these two species happen to meet, at the edge of dahli is a much better ionic regulator than B. the Pixley National Wildlife Refuge in Tulare mackini, at least of Na+, at low environmental County. Habitat water registered next to the high- concentrations of Na+, and as a consequence B. est alkalinity, and the highest pH and TDS, for lindahli is found in soft waters (low alkalinity, any pool known to contain B. lynchi, and it was low Na+) while B. mackini is excluded. However, near the low end of these parameters for B. since these authors show Na+ is treated similarly mackini. Never being ones to shun hypotheses to from moderate to high environmental levels by explain uncommon events, we suggest such non- both species (they conform), apparently different optimal conditions for both organisms may give ion-control physiologies are not what separates neither a competitive edge and both may struggle them throughout much of their range. Fine, you in this habitat. Here is another of those myriad of say; but if separation is generally not in the man- real-world situations that would be fascinating to ner that salts are handled, then what, pray tell, monitor through the season and over the years in does isolate them most of the time? the hope of answering some of our ever-increasing We begin our answer noting that when number of questions! Branchinecta mackini and B. lindahli are found Fascinating stories undoubtedly wait to be told together in our state, their habitats are only mod- concerning the intertwined lives of fairy shrimps - erately alkaline, and are always small, turbid, if only someone would take the time to untangle pools and road-side ditches in the Mojave Desert them! In some cases, particularly in California, it and southern Central Valley. In fact, when found is probably too late, for no one has any idea of alone, B. lindahli typically inhabits small, some- what nameless faces were extirpated before we times tiny puddles usually low in alkalinity. And humans even knew who they were. But in the given its distribution in the most arid parts of the case of two of California's most common and southern half of California, "small" also translates wide-spread anostracans with similar distribu- as short-lived. By contrast, B. mackini, if in small tions, Branchinecta mackini and B. lindahli, there bodies of water, occupies those tending to be are some interesting tales to spin regarding their deeper and therefore longer-lasting, and of greater co-occurrence or lack of same. alkalinity. Perhaps more typical habitats for this Branchinecta mackini, true to its name of al- creature are playa lakes lying in desert basins.

42 Ch. 3. Ecology of fairy shrimps

Some of these playas are very large, and reasona- duce, its clutch size is big, often 3-4 times that of bly long-lasting when filled, like the 20 km-long B. lindahli. In both species, multiple clutches can Middle Alkali Lake located in extreme northeast- be assembled in a season - the number depends on ern California, or Rogers Dry Lake, landing site the pool's longevity that particular year. These for space shuttles (when dry). different strategies of course favor B. lindahli in Ah, the numbers of fairy shrimps that must short-lived pools which may have dried to obliv- filter their way through such large universes - ion by the time B. mackini is able to begin produc- they cannot but boggle the mind! And in those ing eggs. And seeing the comparatively greater numbers lies one of the keys to our present story. number of cysts that can be generated by a popu- Of course reproduction is paramount in order to lation of the latter, it is no wonder that it pre- be successful in the game of life, but then off- dominates in longer-lasting waters. spring must feed, grow, mature, and reproduce Although we do not wish to digress too far again, all with the resources and within the life from our California species, it seems appropriate span of a specific pool. If one species competes to mention that the latter have no monopoly on better and therefore reproduces more, it should this strategy. In his central Texas environs, Den- ultimately swamp the community with its mem- ton (Belk 1991b) watched Branchinecta packardi bers and drive its competitor to extinction. develop to maturity with both small adult and Now consider the reproductive biology of our clutch size in 7 days at Texas summer tempera- two critters in question. As you have come to tures, and thus could complete a life cycle in expect, growth rate and length of time to sexual short-lived rock-pools atop the local geological maturity are related to temperature. According to wonder, Enchanted Rock. The slower-developing Sharon Maynard (1977), during warm falls Streptocephalus texanus, common in longer-lived Branchinecta mackini takes 12-17 days to come to pools at its base, never made it onto the granite sexual maturity. By contrast, B. lindahli requires dome because by the time maturity was attained only 9-13 days. In the cooler temperatures of (11 days and longer), any moisture up there had spring, 21-31 days are needed by the former, been lost to the Texas summer sky. This "Texas while 17-20 are sufficient for the latter. In other two" contrasts with our California cool-water pair words, no matter the temperature, B. lindahli by hatching and holding forth under a hot summer matures about 25% faster than B. mackini. How- sun. These species would have a tough time in ever, there is a price for early reproduction, and California given our inhospitable lack of summer that is one of smaller adult size, with a concomi- rain! And true to this notion, S. texanus has been tant smaller clutch size. Of course the more collected in California only along the furthermost transitory the pool, the fewer are the possible southeast border with Arizona, where Sonoran clutches. Desert thunderstorms occasionally fill basins It seems, therefore, that B. lindahli has a strat- along normally dry washes. And although there egy of allocating much energy early in its life to seems to be no good reason why Branchinecta get to maturity in a hurry, with the consequence of packardi might not also occur in the same area, so small adult size and therefore small clutch size. far as we know, it doesn't! Because Branchinecta mackini spends its energy But back to Branchinecta lindahli and B. early on to grow and attain larger bulk, it cannot mackini and their California homes. Given dif- produce eggs until later. But when it does repro- ferent development times, it is undoubtedly at the

43 Ch. 3. Ecology of fairy shrimps

"overlap" of short- and long-lasting pools where dahli is the versatile fairy shrimp. the two species are found together. In years of In the most southeasterly desert in California, drought B. lindahli predominates, perhaps even the Sonoran, there is a paucity of aquatic biolo- replaces B. mackini if dry conditions continue. In gists searching far and wide for summer fairy years of plenty the reverse may occur. Should the shrimps so the data we have are few. In any seasons see-saw back and forth over time, one can event, Streptocephalus texanus and Thamno- understand why both branchinectid species could cephalus platyurus dwell there in the summer continue to "hang in there" together in spite of heat should thunderstorms dump water on their being closely related competitors. pool sites. Except that these species are both A variation on this theme, which may have its large, both warm-water creatures; and both intol- parallel in California although it has yet to be erant of cold (S. texanus being less so), fairy seen, is demonstrated by two anostracan species shrimp enthusiasts know little about them, includ- far away in the south of Europe. At an elevation ing why, throughout their range, if you find T. of 1,600 m in some secluded mountain-pasture platyurus you usually find with it S. texanus or pools of Italy, Mura (1991b) concluded that some other streptocephalid (Maeda-Martinez et Tanymastix and Chirocephalus, co-occurring fairy al. 1997). But, never lacking for a reasonable shrimps in her snow-melt study pools, shared the hypothesis to be tested, your authors guess that the same hatching stimulus, cold water. Yet, one fact these anostracans are in different genera sug- species or the other would dominate or be exclu- gests structural and behavioral differences which sive in different years. In unwinding the evidence minimize competition and allow coexistence. in this thriller, Mura discovered that when the Certainly T. platyurus is a beast of unique archi- season remained cold, Tanymastix developed tecture (Figs. 7.1, 7.3, pp. 140, 142), but how its faster and matured earlier, of course being of strange form might allow it to cohabit with strep- smaller size than Chirocephalus. Not only that, tocephalids only the creatures of their pools know Tanymastix was killed by abrupt thermal in- at this writing. creases, a not uncommon occurrence in Mediter- In California, the distribution of Thamno- ranean climates. Its co-inhabitant, Chirocepha- cephalus platyurus also extends into the Mojave lus, was unaffected by abrupt temperature Desert, barely overlapping the range of changes, grew at a faster rate in warmer water, Branchinecta mackini. Although the latter can reached larger size, and left a greater number of hatch at summer temperatures, it typically makes cysts than Tanymastix. So, who comes out its appearance in the cold winter waters more "numero uno" in any particular year depends on commonly presented within its range. And even the day-to-day temperature events in these tiny though B. mackini can live in moderate alkalinity, crustaceans' world. Thamnocephalus is found only in waters of low to Because of its wide physiological tolerances, moderate alkalinity; so there is a window of op- and therefore its wide distribution both in and portunity for these species to co-occur, and sure outside of California, Branchinecta lindahli is enough they do, in Troy and Bicycle Dry lakes afforded the chance for many inter-species inter- near Barstow in San Bernardino County. For the actions. Never let it be said that this creature does sake of simplicity, let us once again invoke differ- not take advantage of its opportunities because it ences in adaptive strategies and generic structural holds the record for California (7) as well as else- differences as the most plausible reason at this where in North America (7 more). Truly B. lin- time for their togetherness. 44 Ch. 3. Ecology of fairy shrimps

As a final generalization, predictable, long- non is that when pools are predictable and stable, lasting pools, which occur in areas of snowfall individuals of one species must be better suited and consistently greater rainfall in the Sierra and than those of another to the yearly-repeated suite more northern reaches of California, tend not to of conditions, therefore, in time, the better support more than one species of fairy shrimp. adapted will outcompete others that have found The favored reason for explaining this phenome- their way into the pool (Maynard 1977).

Table 3.1. Coexistence of anostracan species in California

species found swimming with Artemia franciscana B. campestris Artemia monica none Branchinecta campestris Artemia franciscana Branchinecta coloradensis B. mackini, E. serratus Branchinecta conservatio B. lindahli, B. lynchi, L. occidentalis Branchinecta dissimilis none Branchinecta gigas B. lindahli, B. mackini Branchinecta lindahli B. conservatio, B. gigas, B. longiantenna, B. lynchi, B. mackini, B. sandiegonensis, S. woottoni Branchinecta longiantenna B. lindahli, B. lynchi Branchinecta lynchi B. conservatio, B. lindahli, B. longiantenna, B. mackini, "midvalley", L. occidentalis, L. santarosae Branchinecta sp. "midvalley" B. lynchi, L. occidentalis Branchinecta sandiegonensis B. lindahli, S. woottoni Eubranchipus bundyi none Eubranchipus oregonus none Eubranchipus serratus B. coloradensis Linderiella occidentalis B. conservatio, B. lynchi, "midvalley" Linderiella santarosae B. lynchi Streptocephalus dorothae none Streptocephalus sealii none Streptocephalus texanus T. platyurus Streptocephalus woottoni B. lindahli, B. sandiegonensis Thamnocephalus platyurus S. texanus species cysts in same basin, but not seen swimming together Branchinecta lindahli T. platyurus Branchinecta lynchi S. woottoni Branchinecta mackini T. platyurus Streptocephalus woottoni B. lynchi Thamnocephalus platyurus B. lindahli, B. mackini 45 Ch. 3. Ecology of fairy shrimps

What do fairy shrimps eat? Linderiella occidentalis and are sieved out and eaten is presently being determined by Brent Helm We have said in several contexts that anostra- at U.C. Davis. With regards to Artemia, the envi- cans are basically filter-feeders. They are also ronment offers nothing large, for multicellular life described as non-selective particle-feeders. If we (other than the benthic detritivorous brine fly), put those ideas together, we visualize an animal cannot live submerged in its salty habitats. Cer- which indiscriminately removes any kind of par- tain single-celled bacteria, blue-green bacteria, ticle from the water that its suction currents can and green algae, all very tiny creatures, must bring in and its filter size can retain, be it bacte- therefore suffice for Artemia's nutrition. In order rial, plant, animal, detrital, fine sand, or glass to obtain these cells, a filter with a small enough beads offered by some researcher. Digesting its mesh to sieve out such food was obviously evolved treasures is another story. Because of their undis- for the job. Ah, adaptation! criminating eating habits, fairy shrimps are best Now, what about the other extreme? How called omnivores, or opportunistic feeders, eating large a particle can Artemia collect and ingest? whatever is available. But what are the sizes, or Schrehardt (1987) writes that maximum particle variety of sizes of particles, retained and eaten by size increases from 10 ^m for early nauplii, to 30 different fairy shrimp species? The simple answer jim for mid-stage larvae, and 50 jim in adults. is no one knows! The more involved answer Because all life stages filter bacteria, it appears which follows deals with what few data exist. that mesh size does not increase with growth of Size of mesh or filter in anostracans has been the animal. Also, it looks as though the ability to determined for only 6 species that we know of, consume larger and larger particles as Artemia and only two are found in California. One, Lind- increases in size may be determined by oral di- eriella occidentalis, has the smallest filter re- mensions, and the effectiveness of mandibles in corded - an incredibly tiny 0.3-^im intersetal dis- reducing larger particles or organisms to pieces tance (Helm in prep.). Not much larger is the that fit into the mouth. brine shrimp Artemia franciscana with a 0.5-^im When hollow glass balls of a variety of micro mesh, and, with it, life stages from nauplius to sizes were suspended in an aquarium and filtered adult retain individual bacteria (Schrehardt 1987). by Streptocephalus proboscideus (an African That's small food! But being so fine a mesh, it is anostracan with a mesh size of 3.5 jim), the exact not difficult to imagine these micro feeding same trend was recorded as for Artemia. Here the mechanisms clogging if the animals' aquatic young engulfed particles from 5 nm (the smallest world was loaded with particles much larger than presented) to 17 jim, while adults managed parti- 0.3-0.5 nm. Perhaps we have here part of the cles from 5-79 nm (Brendonck 1993). reason that L. occidentalis dwells overwhelmingly Well, how about the other Californians? Do in deep, clear-water vernal pools (Helm 1998) we have any ideas about what they can stuff into where vegetation impedes mixing thus the stirring their mouths? The contents of the guts of up of clays, and Artemia lives in brines where Branchinecta mackini were extracted by Maynard clays cannot remain suspended because they pre- (1972), and amongst the treasures found were cipitate if TDS exceeds about 3,000 ppm. Ah, algal cells that ranged from 10-50 jim. Maynard physics! was attempting to compare the diet of B. mackini What tiny or big particles exist in the homes of with another branchinectid, B. paludosa. She

46 Ch. 3. Ecology of fairy shrimps

exopod

epipod

preepipod

Fig. 3.1. View of the anterior surface of the right fifth phyllopod (leg) of a male Branchinecta longiantenna. The numbers 1-6 mark the endites. Endites are inwardly (medially) directed lobes of the unbranched basal part of the leg, the basipod. Scale = 1 mm.

47 Ch. 3. Ecology of fairy shrimps commented that the latter had a coarser, but un- number of species supplement their feeding by measured, "filtratory net", a situation which corre- turning over (remember, fairy shrimps swim on lated with cells 92-100 jim in size in its gut. Fi- their backs) to scrape the flocculent bottom de- nally, Daborn (1979) counted twice as many setae posits into suspension with their beating phyllo- in the filter area of an appendage from B. mackini podia. Some return to their normal swimming as compared to one from B. lindahli, suggesting a position with a load of scrapings between their finer mesh-size for the former. Problem! The B. phyllopodia, others swim through the sediment lindahli he measured were half the length of the cloud, apparently filtering appropriately-sized B. mackini. So naturally, for these data to be most particles from it. useful we need to know whether or not setal num- So, what are these particles they filter and en- ber and spacing change with an increase in ani- gulf, and how nutritious are they? In a pool with mal size. "clean", clear water the particles are largely phy- How different are the size-ranges of particles toplankton and bacteria, but they must include filtered and ingested by the various anostracan protozoa, rotifers, and tiny larval forms of a vari- species? A fascinating study which would begin ety of species. From present information, we to answer this question might involve the follow- conclude that individual bacteria are probably not ing. Into one aquarium stocked with similar-sized captured by the sieves of most species of fairy fairy shrimps of different species, and a second shrimps because mesh-size is too coarse. Much of with different-sized individuals of the same spe- the animal material ingested probably gets fully cies, mix an appropriately wide size-range of glass digested. By contrast, phytoplankton cells are or plastic beads (industrially available; Brendonck surrounded by a cellulose cell wall which is not 1993). After the animals stuffed themselves for digestible by animals, but the wall, is a rather awhile, ingested beads could be removed from small fraction of the total cell volume and is per- their guts and measured under a microscope. The meable to a fairy shrimp's digestive enzymes. minimum and maximum diameters, and the size- Therefore, this array of foods, being mostly di- ranges thus established for each age and species, gestible, is undoubtedly a very nutritious smorgas- could then be compared to the measured filter bord for anostracans. mesh-size of each. Such a study, possibly highly In a pool with muddy water, insufficient light instructive about how the differences in food re- penetrates to allow photosynthesis. Particles pres- sources utilized by each species could minimize ent may include the animal types already men- both inter- and intraspecific competition, has not tioned and bacteria, but phytoplankton is absent. been done. Will someone step forward to pursue Particles in greatest abundance are the clays that this one? Whoever does, try to incorporate a great muddy the water. Clay is inorganic and indi- idea our editors proposed, color-code the beads for gestible. So what supports the energy require- size, for that would make your evaluation so much ments of the fairy shrimps and other community easier! members? The answer is, directly or indirectly, Of course fairy shrimps are constant swim- the remaining type of particle, detritus. mers, so what they filter comes from the water Detritus is an exceedingly important particle through which they navigate - at least it does for type in pools, be they muddy or clear. It is dead Artemia and Linderiella occidentalis. Although organic matter, largely of plant origin. Its nutri- we do not know how general the situation is, a tious fraction has already been used by someone

48 Ch. 3. Ecology of fairy shrimps

or, as with tea leaves, leached into the water as during times of excessive rain or flood, and pos- dissolved organics. What remains is composed sibly wind, are undoubtedly important agents of largely of cellulose and lignin, which are not di- detrital transfer. Where surrounding vegetation is gestible by macroscopic life. Two questions are tall, leaves and branches may be blown down into immediately obvious. First, if these materials are a pool. In the desert, flash floods move not only not digestible by fairy shrimps and others, why are fantastic quantities of rock particles, but the rag- we talking about them? And second, if the pool is ing water also picks up leaves, twigs, even bushes turbid and cannot support photosynthesis, where that have accumulated in washes, and reduces does detrital plant material come from anyway? them to smaller pieces as it grinds its way down- One question at a time, please! hill to the collection basin, often a desert playa, Although the "large" creatures we visualize as below. making up the pool community cannot digest Irrespective of whether a pool is turbid or cellulose and lignin, bacteria and fungi can. By clear, there is yet another mechanism for trans- themselves, detrital fragments are about 5% pro- porting detritus. In today's California, cows, tein, but after several days in water they are colo- horses, and rabbits, probably in that order of nized by bacteria and fungi and the protein con- abundance, are the main big grazing animals that tent of the "combo" rises to about 25% (Cummins come to pools to drink. Oh, yes, throw in a few et al. 1989). To paraphrase Ken Cummins, detri- sheep as well. Historically, elk, pronghorn, and tal fragments are like saltine crackers - not much deer roamed the California range instead, or go nutrition by themselves, but when spread with back a step further in time and add mastodons, peanut butter they become a very wholesome food. camels, giant ground sloths, and all other such So, the organisms that can filter detritus particles creatures that are no longer with us. All but the from the water and eat them digest the nutritious rabbits certainly did not or do not hesitate to wade bacteria and fungi. The still indigestible, but on in to take a drink. In order to make room for somewhat more fractionated, cellulose and lignin that wet, cooling elixir, these animals are prone to remains are then defecated into the pool where dump their unusable products into their drinking colonization begins anew. Isn't there a well- water, yea into the fairy shrimp habitat! Their known saying that goes something like "from de- urine is a fine nitrogen source, and one that can be tritus to detritus"? Whatever the literary equiva- converted by bacteria to ammonium or nitrate and lent, detrital cycling is real, and very important! used by those bacteria, and algae, for growth; the All that remains now is to get "colonized detri- "road apples", "cow-pies", fecal pellets, call them tus" into the water in appropriately sized particles what you may, are fine sources of partially pulver- and the fairy shrimps can "chow down". Mixing ized organic matter. And anyone who has walked action of wind, and stirring up of the bottom by through a pasture or along a favorite fishing animal activity, including scraping by some anos- meadow knows the prodigious amount of proc- tracans, are the causative agents. With regard to essed detritus this source can move (pardon the our second question, detritus which originated pun). outside a pool can be brought to it in several ways. There is yet another story that merits telling. In areas where there is little vegetation to impede Although the process undoubtedly applies to all movement, wind may blow dead material along muddy-water habitats, the details were worked out the ground, only to have it trapped in a water- with Branchinecta mackini in a desert playa, filled basin. In grassland areas, overland flow Rabbit Dry Lake, by Mike Patten and Louis Rap-

49 Ch. 3. Ecology of fairy shrimps poport (1980), two students who were working several days of wind-mixing of water over playa with Clyde. After a steady but non-drenching rain soils are usually necessary to raise the dissolved formed shallow pools in the basin without the aid salt concentration to a level that inhibits further of significant run-off, analyses showed that playa hatching. water contained little particulate organic matter. Mizutani (1982), using Branchinecta longian- Interestingly, and fortunately, no fairy shrimps tenna (thinking it was B. mackini), did some hatched into these food-less waters. Shortly after creative lab work to establish what the animal the pools dried, a heavy winter storm created flash eats. He labeled a common sugar and an amino floods which brought water, mud, and organic acid, both of which occur dissolved in playa water, particles from the surrounding mountains to fill with radioactive tracers. These materials suppos- the playa. Fairy shrimps now hatched and lived edly are leached from detritus brought by flash happily ever after, well, at least until the particu- floods. Physicists tell us that dissolved particles late organics ran out or the pool dried up. And are charged particles, and both of these organic why didn't the shrimps hatch in the first instance? molecules have positively charged ends. Clays, Was it related to no food? We doubt that one; just although not dissolved, are so small they too have how could a cyst determine whether or not food surface charges, theirs being negative. Ah ha! particles were out there? Or, was it the non- The clay particles, present in such massive num- drenching rain? Come on now, how do fairy bers that they make the water muddy, attract and shrimp cysts distinguish between drenching and bind dissolved organics, and "hungry" bacteria non-drenching precipitation if both supply pud- cluster around and grow on these nutrient-rich dles, pools, and playas with water? surfaces. Such a layering of goodies makes a par- Back in Chapter 2 we explained that the ticle large enough for at least some fairy shrimps conditions which stimulate hatching of Branch- to filter, and filter they do, for the radioactive or- inecta mackini are known, and were also worked ganics were detected in their bodies. Although out on the Rabbit Dry Lake population. Remem- the clay center of such a concretion is non- ber that fresh water, or at least a sudden decrease digestible, the "peanut butter" on its surface, and in dissolved salts, is required to begin coaxing dissolved organics held underneath, make for a nauplii from cysts. However, when the water's nutritious morsel. So, fairy shrimps propel them- TDS exceeds 1,000 parts salt to a million parts selves through their dark, turbid milieu, seeing water (1,000 ppm), hatching is inhibited. If we little, darting in another direction when they apply this information to the observations of Pat- bump into something, but continue filtering nutri- ten and Rappoport, we realize that the steady light tious "mud" (or should we also call it a type of rain which added water drop by drop to the detritus?) from the water. Not far down the gut its playa's salty soil, plus the constant mixing action contents are acidified, and the charged organics of wind on water, assured a high salt content in are disengaged from the clay. The former, and the pools that formed. The result, of course, was the bacteria, are digested and absorbed, the clays inhibition of hatching. In contrast, when flash are moved on and out, ultimately to become sus- floods descend the mountain slopes and fill the pended particles once more, allowing the process playa rapidly, although muddy, the water is large to begin all over again. in volume and low in TDS. Hatching is therefore You may think we have spent an inordinate stimulated. Because of the large volume of fluid, amount of time talking about detritus and who

50 Ch. 3. Ecology of fairy shrimps eats it, for after all your favorite pool is probably phyllopodia together, the tips of which then over- not the color nor the consistency of a chocolate arch the food groove, and at the same time flexing milk shake. For most folks, it is more romantic to its abdomen over its appendages, our predator think of living things eating living things under attempts to trap its much smaller prey in this clear blue skies and in crystal clear water. How- "phyllopodial basket" (White et al. 1969). If it is ever, to put detrital food chains into perspective, successful, the niceties begin with the predator consider that probably as much as 95% of an moving the prey forward with the spined bases of aquatic community's energy flow ultimately its appendages to the mouth area where it is passes along such a route; that's only about 5% "processed" by the mandibles for ingestion. for the romantics. Pretty impressive, or disquiet- Armed with sharp denticles, mandibles not only ing; depends on how close your esthetic and eco- pierce the food when they close, but crush and nomic views are to ecological reality! move it forward as they rotate toward the mouth. And speaking of ecological reality, you already Thus Fryer (1966) describes these mandibles not know our description of anostracans as being fil- as tearing or chewing devices, but as "crushing ter-feeders is an over simplification, for many rollers". For the trapped fairy shrimp or other fairy shrimps also scrape detritus from pool bot- crustacean food item, this process is "the end of toms. Further, there are two species which terror- the line" as the punctured and mashed body is ize the crustacean world with carnivory. One, ingested whole. Robert Brown reminded us that Branchinecta ferox, lives in North Africa and although the prey may have been moved into the Europe and is a filter feeder when small. How- gut in one piece, it had undoubtedly lost a signifi- ever, when a length of perhaps 15-20 mm is at- cant amount of nutritious body fluid. Remember, tained, the animal develops such strong suction this fluid, or hemolymph, circulates in large body currents that it is able to draw in copepods and spaces, not in closed vessels. The pressure which cladocerans (Fryer 1983). Because this beast causes circulation also keeps the body "pumped grows to lengths of at least 45 mm, it feeds on up" thus giving it form, as with a balloon. So, these animals for a goodly portion of its life. when our predator punctures its food item and Branchinecta gigas is the other carnivorous hemolymph rapidly spews out, the full caloric anostracan, and its distribution includes the Mo- value of the prey goes unrealized. Because B. jave and Great Basin Deserts of California. This gigas cannot return to the drawing board to cor- animal is giant enough that it feeds on other fairy rect this problem, it gets busy groping for more shrimps, particularly B. mackini, but B. lindahli, prey to meet its energy needs, and grope effec- as well as cladocerans and copepods, may be tively it does! Anderson (1970) demonstrated this significant food items as well. It turns out that B. fact with a simple and tidy experiment in which gigas lives only in highly turbid habitats and thus he placed 1,040 cladocerans, 200 copepods, and is not a visual predator; in fact, it has by far the 20 B. mackini in 3 L of water with a single 75 smallest eyes in proportion to body size of any mm-long B. gigas female. After 200 hours in this fairy shrimp. Because it does not create suction dark, 10°C meat market, only the female predator currents that are strong enough to draw in large was left swimming. prey, this fearsome beast swims alertly through its Perhaps when food resources become scarce B. murky medium and reacts immediately upon gigas casts around for alternatives; at least Fryer contact with a potential meal. By drawing its (1966) thinks so, for he suggests that scraping is

51 Ch. 3. Ecology of fairy shrimps used to supplement its diet. And just so you know anostracans' body cavities. Once filled with who- this beast seems to take advantage of every option ever it was, the fairy shrimps succumbed. As has to enjoy a meal, Belk and Ballantyne (1996) ob- been said before, there needs to be bread on every served some of these characters clustered around a table! wad of Spirogyra apparently "...pulling at the al- So much for pleasantries, let's get down to gal mass with their phyllopods." That they feed naming names of those who eat whole fairy on this kind of material at times is suggested by shrimps! How's this one: giant fairy shrimp, so the fact that algal filaments were found between named because it is! We just told you about this the mouth parts and in the gut. Those times must behemoth's eating habits, but feel free to check be few, however, for as we have noted, B. gigas back on its culinary artistry. typically lives in waters so turbid that algae can- Another predator of anostracans is the tadpole not grow. shrimp (Fig. 1.1, p. xiv). There are four species of these "Jurassic Park" creatures in our state. What eats fairy shrimps? Three live in turbid, desert alkali playas like our giant friend Branchinecta gigas, the fourth dwells The old adage that "those who live by the in pools of low dissolved solids in the northern sword, die by the sword" even has meaning for Central Valley. Two of the desert alkaline-lake anostracans. Although these graceful and seem- tadpole shrimps share the same food, B. mackini. ingly passive creatures are hardly the sword- However, they appear to divide feeding opportu- carriers for which the statement was written, they nities in these places by season. Lepidurus lem- do live by eating considerable quantities of living moni eats B. mackini in winter and spring waters. things. And, in their turn, they die by the Triops newberryi must "chow down" on them, "swords" of birds, bugs, and beetles. Some also possibly Thamnocephalus platyurus and who fall prey to jaws of relatives - another fairy shrimp knows what else, during summer (no one has or a tadpole shrimp, even dragonfly larvae, occa- ventured into the heat of the Mojave at opportune sionally fish, amphibians, and, yep, humans. moments to find out). About who eats them from the inside (parasites) The intriguing question (yes, another question) we know next to nothing except that they do fall is: how do B. gigas and L. lemmoni, whose distri- prey from within. Amat et al. (1991) and Jarecka butions in California overlap significantly, divide (1984) noted that the brine shrimp Artemia, and winter and spring playa waters between them, the freshwater fairy shrimp Branchinecta gaini, given that they share B. mackini as their major can serve as intermediate hosts for the cyst stages food? Before the 1992-1993 rainy season we of hymenolepid tapeworms. The presence of these knew of no records that these species co-occurred, cysts has no effect on survival, but it does lead to and we wondered who out there would find out castration, obviously a factor in the size of the why? Well, we still don't know why, but Marie next generation of shrimps. Long-time anostra- Simovich and Richard Gonzalez (1993) found can enthusiast Robert Brown collected a pot full of both species inhabiting sites scattered across Ed- Branchinecta lindahli near Soda Lake in San Luis wards Air Force Base in the Mojave Desert. In 8 Obispo County and returned them to his lab at of those pools, one species or the other was pres- CSU San Luis Obispo. There he watched as an ent; in 12 of them both occurred. However, in unknown micro-organism grew and occluded the examining the Simovich-Gonzalez data, we noted

52 Ch. 3. Ecology of fairy shrimps that B. gigas was often present from November to it and therefore occur there. In like manner, the January, while L. lemmoni did not usually appear more distant the island the fewer in number are until January or March and remained in the pools the species in residence. Why talk of islands later into spring, in several cases much later. when our concern is puddles? Well, such places Perhaps thermal cues separate the hatching times are aquatic "islands" in a sea of land, and if those of the two predators. When the earlier-hatching pools are "next door" to permanent water, as is Branchinecta gigas appears, its nutritional needs relatively common in the northern two-thirds of are met by B. mackini. As the B. gigas popula- the Central Valley and the high Sierra, organisms tions bow out, B. mackini is then fed upon by the which inhabit the latter find the pools in a short later-appearing L. lemmoni. time. In areas where permanent water is scarce, Lepidurus couseii has recently been recorded and temporary pools are often quite distant from a in the Great Basin Desert of the far north-east of permanent source, colonization is slower, possibly our state, and although it has not yet had its eating even out of the question for most species. A broad habitats described, we'll bet it too eats anostra- brush would paint California's southern moun- cans. tains and deserts with this color. Golly, desert waters seem to have phyllopod Water birds, being highly mobile travelers, predators of fairy shrimps galore; but how about have got to be amongst the fairy shrimp's biggest the rest of California? The fourth of the state's concerns even in some of the most distant tadpole shrimps, Lepidurus packardi, dwells "islands". These birds are large and always hun- mainly in the northern and eastern Central Valley. gry. They move easily into a habitat, take what Its distribution thus overlaps those of they can get, then depart. In desert areas, Ameri- Branchinecta lynchi, Linderiella occidentalis, and can avocets are a particularly common sight several uncommon fairy shrimp species. In a wading in turbid, alkaline waters and swishing Sugnet and Associates study (1993), Lepidurus their sword-like beaks to and fro. Whatever they was taken in 345 of about 3,100 locations hit they attempt to grab. Given fairy shrimps' checked, and at least 40 of these were occupied by place in food chains, and thus their numbers, they L. occidentalis, many fewer by B. lynchi. Al- are undoubtedly the most common morsels en- though we know nothing about the interactive countered by the avocet's beak. Kildeers, wading private lives of these creatures, we must assume birds which also are known to eat fairy shrimps Lepidurus packardi enjoys eating tasty anostra- (Proctor et al. 1967), are a common sight around cans whenever they co-occur. rain pools throughout California, and Lenz (1987) Other than those organisms exposed above, describes gulls and grebes as being avid eaters of there are no others that prefer munching on fairy Mono Lake's resident brine shrimp Artemia shrimps who dedicate their whole lives to pools. monica. But, like children and relatives who take advan- Swanson et al. (1985) and Eldridge (1990) tage of abundance, then leave when supplies run have written that northern pintails and mallards, out, there are predators that fly, walk, hop, or which come to rest on prairie pools along the swim into pools when such pastures are plentiful; midwestern flyway, feed on fairy shrimps because then fly, walk, hop, or swim out (if possible) when they are one of the first invertebrates available pool resources dwindle or water disappears. once the temporary waters form. Northern shov- Studies with islands show the smaller the is- elers and blue-winged teals also are noted to have land, the fewer the colonizers that happen to find significant portions of their diet composed of 53 Ch. 3. Ecology of fairy shrimps anostracans. Undoubtedly these and other ducks eat fairy shrimps they do, at the clocked rate of that wing their way over California find fairy 2.06 individuals per notonectid per hour shrimps equally significant to their diet, but we (Woodward & Kiesecker 1994). are unaware of any research done in the state on Predaceous diving beetles are another common the feeding habits of ducks. What we are aware of sight. Like the bugs, they too carry an air store is that "The wetlands of the Central Valley pro- and also hang from the surface film, then swim vide wintering habitat for 19% of the wintering rapidly through the water in search of prey! waterfowl in the continental United States. They There are a variety of species and sizes, but some support some of the highest densities of waterfowl fall into the size range of anostracans, and some in the country. Nationally, these are the highest are even much larger, both as larvae and adults. priority wetlands for preservation of wintering Although both life stages feed in the same man- habitat." (Secretary of Interior 1994). We also ner, larvae are particularly fascinating beasts. know that the Central Valley is California's rich- The mandibles are magnificently large, curved, est fairy shrimp country. We suggest that these and sharp. In fact, they are hollow and are not two facts are not unrelated! Further, an observa- used in chewing. Like ice tongs, they close on tional study of use by birds of vernal pools on the their prey and impale it. Then digestive enzymes Santa Rosa Plateau in western Riverside County are pumped into the body of their food through (Baker et al. 1992) demonstrated that, in the these hollow structures and, when digestion has larger pools, mallards, northern shovelers, and reduced the prey's internal parts to a slurry northern pintails are frequent guests. In addition, (exoskeletons are not digestible), it is sucked in green-wing and cinnamon teals are common, and through the beetle's mouth with gusto. Bob the list goes on to include gadwalls, American Brown points out that if the beetle is in no hurry, wigeons, and ring-necked ducks. Since the waters meaning that it must make the most efficient use of these larger pools are plied by fairy shrimps, we of limited food reserves, this feeding strategy is a doubt the ducks come merely to float unaware of tidy way to go. However, he has watched many a the shrimps' presence. For more information on diving beetle grab, pierce, suck, and run (swim avian uses of California's ephemeral pools, take a off), suggesting that if food resources are plentiful, look at the review by Joe Silveira (1998). sucking a fairy shrimp's hemolymph, rather than Although insects are reasonable fliers, distance waiting around for digestive enzymes to reduce from their permanent-water refugia to temporary tissue to a slurry, is the more efficient way to pro- pools becomes a problem. Only adult insects fly, ceed. so they are the colonizers, and aquatic bugs and If the pool is long-lived enough, offspring of beetles are the most common of these. Having these air-breathing colonizers may be seen in flown into the soup of a pool, they spend their numbers, as may the aquatic larvae (also called time diving, often to some depth, in search of nymphs or naiads) of dragonflies and damselflies. prey. Of the bugs, the most common are Adults of the latter groups are terrestrial insects, backswimmers (Family Notonectidae). Like all and are seen flying in the vicinity of pools looking bugs, these have mouth parts for piercing their for food and mates, but they are also there to lay prey and sucking it "dry". Notonectids are aqua- eggs in the water. Because the larvae are aquatic lungers, so they may be seen hanging from the and have gills, they always remain submerged, surface film where they recharge their air stores, usually clinging to a surface, be it the bottom or then dive after food, including fairy shrimps. And aquatic vegetation. Although they move from

54 Ch. 3. Ecology of fairy shrimps place to place, they are not great swimmers like cause midge larvae are usually somewhat buried beetles and bugs, and thus are more the wait-see- in bottom sediments, and fairy shrimps swim, and-pounce type of predator, some pouncing on little is the opportunity for such a predator-prey fairy shrimps. interaction to occur. Knowing this, Tim moni- All these predatory insects must see to feed. tored the encounter until the midge had killed and Should the pools become occluded, vision is im- consumed half of the fairy shrimp. How did a paired, their way of life is obviously limited swimmer cross paths with a non-swimmer? Per- (Woodward & Kiesecker 1994), and these crea- haps you will remember that some species of fairy tures disappear. Another way of saying this is shrimps have a habit of mucking around that, if pools are muddy, visual predation is out of (scraping) in bottom sediments. Undoubtedly the question, and finding prey by bumping into it Graham's fairy shrimp was following that passion is "the way to go"! So we have come full circle in when the midge trap was sprung. Perhaps a more our feeding story; we are back to fairy shrimps orthodox paraphrase of a common expression is and fairy shrimp-relatives eating fairy shrimps in appropriate here: "predation happens"! the darkness of muddy pools! One last comment As mentioned in the "Community" section of though about such environments. Because this Chapter 3, fishes may occasionally enter anostra- bump-and-feed life style not only depends on a can habitats when flooding occurs, be it natural or high density of prey but a large enough prey agricultural. McCarraher (1959), Pereira and population to support a predator population, small Gonzalez (1994), and Zemmouri (1991) have pools and puddles, particularly those with small caught various fish species in the act and recorded numbers of anostracans, do not sustain the preda- it for posterity. When such an event occurs, the tor level of this food chain. However, should the opportunistic fish will certainly eat fairy shrimps small pool be clear, it may also contain the visu- until they cannot find more, until they find their ally-feeding bugs and beetles who can snatch up way out, or until they perish with the pool's dry- conspicuous and tasty morsels, then leave to gain ing. We can safely say that fishes are of little im- sustenance elsewhere. portance to modern-day fairy shrimp ecology; We have an uncommon but wonderful little however, in the vast past of evolutionary time, example of free-market opportunism to share with after fishes first came into being, they must have you, although it is certainly insignificant to fairy encountered environments filled with tasty fairy shrimp biology. Our story involves a midge, a shrimps. Kerfoot and Lynch (1987) and Wagele relative of the mosquito. As larvae, midges, like (1992) reason that the evolution of more versatile mosquitoes, are aquatic. Unlike mosquitoes they predatory methods by fish (read this over-kill by don't hang from the surface film; rather, they live fish), particularly the development of suction on or just under surfaces, usually of the bottom feeding, ultimately exterminated fairy shrimps sediments. And also unlike mosquitoes, some of from all permanent waters by Mesozoic times, them are predators. Anyway, Tim Graham leaving anostracans only ephemeral pools as (1994), a U. S. Biological Service scientist, was refugia against extinction. peering into potholes (the water-filled variety) in Frogs, toads, and salamanders are also not Utah when he noticed a fairy shrimp moving usually thought of as inhabitants of temporary about erratically. "Good reason for such panic", waters. However, in damper areas of California, he undoubtedly thought when he saw a midge and in wetter weather, adults of these creatures larva clamped on the fairy shrimp's head. Be- may migrate to pools to lay eggs, and, along with

55 Ch. 3. Ecology of fairy shrimps their immatures, use these wet places as tempo- spade-foot toad come in both predator and omni- rary feeding sites. Frogs feed both above and be- vore morphs (forms), sometimes in the same pool. low waterline, and how effective they might be in In a fascinating piece of work by David Pfenning utilizing fairy shrimps is unknown, but instances (1990), via astute observations and experimental of young bullfrogs filling their guts with tadpole manipulations he showed that "...morph determi- shrimps are known from the Vina Plains near nation depends on the ingestion of shrimp. .. If a Chico (Federal Register 1994). Anostracans are a critical number of shrimp were ingested, the tad- part of the diet of at least some salamanders and pole developed into a carnivore; if not, the tadpole their larvae. We say this, even though no one has developed into an omnivore." And who were gone public with such information from Califor- these body-building New Mexican "shrimps"? Ah, nia, because several scientists have spied on these those tasty tid-bits (steaks?) Streptocephalus tex- beasts elsewhere (e.g., Sprules 1972; Thiery 1991; anus and Thamnocephalus platyurus, that's who. Woodward & Kiesecher 1994; Woodward & By the way, Simovich et al. (1991) also agree that Mitchell in prep.) and found both adults and im- fairy shrimps are "...an important component of matures to include fairy shrimps in their food the natural diet..." of spade-foot toad tadpoles in supply. Finally, in California's more southern Arizona; so this issue seems to be settled! reaches where spade-foot toads hang out, they and The last of the vertebrate predators, with col- their sometimes predaceous tadpoles may benefit lecting equipment and behaviors capable of sam- from fairy shrimp feasts. Although no one has pling both turbid and clear waters alike, are hu- told of this drama being played out in California mans. Among them of course are those of us who either, once more we rely on Woodward and study fairy shrimps, as well as the individuals who Mitchell (in prep.) for the juicy information that use these graceful creatures for the myriad of pur- adult spade-foots will in fact feed on Strepto- poses already revealed in the Chapter 1 section cephalus texanus. Interestingly, tadpoles of the "What good are fairy shrimps?"

Fig. 3.2. Cysts of the California species of Eubranchipus. From the left, E. serratus 0.38 mm diameter cyst, E. oregonus 0.37 mm diameter cyst, and E. bundyi 0.31 mm diameter cyst. SEM photographs by Graziella Mura, Universita degli Studi di Roma "La Sapienza", Italy.

56 Chapter 4

STATEWIDE DISTRIBUTION OF FAIRY SHRIMPS

Fairy shrimps aren't everywhere in find no anostracans or tadpole shrimps west of the California Sacramento River from Yolo County north. An intensive survey by Sugnet and Associates, California is certainly rich in anostracans. In Roseville, (1993), apparently blanketing all of the fact, we can rightfully brag that, of the 23 known Central Valley and beyond, and including private species that call our state home, eight are found lands often difficult to sample because of limited only here (and in a northern sliver of Baja Cali- access, led to essentially the same conclusion. fornia, Mexico). These statistics are both North Further, they found the same general absence of American and world records for the number of anostracans and notostracans in the Central Val- species of anostracans occurring in a comparable ley west of the San Joaquin River from Alameda land area. No matter the reality, we sometimes County south. Shawn Gallagher (pers. comm.) hear silly and uninformed rhetoric about fairy wrote of his impression of few fairy shrimp loca- shrimps on radio and TV by individuals hoping to tions west of the Sacramento River when he sent harvest political hay. The printed page may be no us an unpublished "Vernal Pool Survey" (Alex- different, as exemplified by the grossly inaccurate, ander & Gallagher 1993), done while he was a almost hysterical disservice to truth by some uni- student at CSU Chico, demonstrating that of 36 dentified author of a Wall Street Journal article pools visited west of the river and south of Red dated October 17, 1994. The thesis of the article, Bluff only 10 contained shrimps, all Branchinecta entitled "A Fairy Shrimp Tale", was that all lynchi. One might argue that there are few fairy shrimps are the same, and all live in mud holes, shrimp sites west of the Central Valley's two main and because mud holes are everywhere, fairy rivers because development has "done'em in". shrimps are everywhere. Ignorance is bliss they However, there is no less development east of the say, but in spite of this writer's bliss, FAIRY rivers where the great majority of the Valley's SHRIMPS AREN'T EVERYWHERE! anostracans are found, so this is an unsatisfying True, we have described our little subjects as suggestion. "the symbol of rain pools", but they are not in Finding out what species reside on the less de- every rainpool, or mud puddle, or stock-watering veloped lands of wildlife refuges, no matter their hole, or road-side ditch, or even everywhere in location, would be a worthwhile endeavor since California as is attested to by Map 4.1 (p. 58), a historically these places have gone largely unex- compilation of all known locations of all of our plored. To its credit, the Federal Government has state's fairy shrimps! Don Wootton used to tell recently developed an interest in wetlands, and your first author that even in the heart of the fairy shrimps, so managers of National Wildlife Central Valley's fairy shrimp country he could Refuges (NWR) have begun to look for species

57 Ch. 4. Statewide distribution of fairy shrimps

Map 4.1. Plot of all our records of occur- rences of fairy shrimps in California. t; /I •••

X \\ A \ L 'WU \

1 ^

V\

w ' . . J-X

V }: - J v. V o o

•r

< ^m

miles 0 10i0 0 50 100 kilometers

58