AMER. ZOOL., 28:115-124 (1988)

Systemic Respiratory to Air Exposure in Intertidal Decapod Crustaceans1

PETER L. DEFUR Department of Biology, George Mason University, Fairfax, Virginia 22030

SYNOPSIS. The responses of intertidal decapods to emersion are closely related to the particular conditions of emersion, yet all members of this group of face the problems of water shortage and internal hypoxia during air exposure. Several Downloaded from https://academic.oup.com/icb/article/28/1/115/169154 by guest on 23 September 2021 exhibit modification of normal ventilatory activity and this response seems to enable these to take up seawater from the substrate. Other crabs have specific morphological adaptations permitting recirculation of water from the exhalent apertures back into the gill chamber. The hemocyanin of some species has a higher affinity for oxygen, and this difference may be more prevalent in tropical animals. The higher oxygen affinity undoubt- edly compensates in part for the lower internal oxygen tensions during air exposure. Structural specialization of the branchial apparatus may prevent the gill lamellae from adhering together, a process which reduces the surface available for gas exchange. There is a wide range of responses to emersion and yet relatively few specific adaptations. Some species are able to merely tolerate air exposure, while others are able to more fully exploit the habitat.

INTRODUCTION may limit the comparisons. Truchot This review examines systemic adapta- (1975) for example, exposed shore crabs, tions of the gas exchange system of inter- Carcinus maenas, beneath a layer of sea- tidal decapod during air expo- weed, and Taylor and Butler (1978) sure (emersion), and both ventilatory and exposed the same species without sub- circulatory processes will be discussed. Res- strate. Further, some of these species are piration includes oxygen uptake, carbon small, precluding sampling of hemolymph dioxide excretion and acid-base balance, or measurement of certain functions such as cardiac output. and because acid-base balance and CO2 excretion are covered by Truchot (1988) Intertidal zones are spatially and tem- and Burnett (1988) in this symposium, the porally diverse environments. For exam- emphasis will be on oxygen. Based on recent ple, Truchot and Duhamel-Jouve (1980) reviews by evolutionary biologists (see measured diel patterns of both hypoxic and Cisne, 1982), the assumption is made that hyperoxic conditions in the same tide pool. intertidal decapods are basically aquatic Truchot (1988) has described some of the species which are on the edge of their factors which account for these variations. ancestral environment, that is, there are Other environmental factors such as tem- no intertidal decapods which came from perature, salinity and amount of interstitial the land. This review is based on data from water may change during emersion. Some surveys such as Gray (1957) and Mangum characteristics, including the type of sub- (1982) and from several in depth studies strate, the slope of the beach, the amount of individual species {e.g., Truchot, 1975; and type of vegetation and the tidal flux Taylor and Butler, 1978; deFur and differ among sites. These factors affect McMahon 1984a, b\ O'Mahoney and Full, either the availability of water to an animal 1984). Differences in the experimental in the intertidal zone, or the quality of that conditions such as the duration of emer- water. Water availability is an important sion, the substrate and the handling of the limiting factor for terrestrial animals, as McMahon and Burggren (1979) concluded for physiological functions of terrestrial hermit crabs, and it is probably even more 1 From the Symposium on Mechanisms of Physiolog- so for strictly aquatic species. The variation ical Compensation in Intertidal Animals presented at the in environmental conditions in intertidal Annual Meeting of the American Society of Zoolo- gists, 27-30 December 1985, at Baltimore, Maryland. zones undoubtedly determines the wide 115 116 PETER L. DEFUR

range of responses of intertidal decapods, animals. The shore , Carcinus maenas, as deFur and McMahon (1984a) pointed has received considerable attention, and out. small animals readily leave the water Oxygen uptake and transport in deca- (Atkinson and Parsons, 1973), but large pod crustaceans have recently been crabs may have to be forced out of the reviewed by several authors (Mangum, water by hypoxia (Taylor and Butler, 1978; 1983; McMahon and Wilkens, 1983), and Depledge, 1984). , Orconectes rus- the reader is referred to these works for a ticus, also leave hypoxic water to ventilate

more detailed treatment of the subject. the gill chamber with air (McMahon and Downloaded from https://academic.oup.com/icb/article/28/1/115/169154 by guest on 23 September 2021 Briefly, the scaphognathites, located in the Wilkes, 1983). Several intertidal species exhalent channels, move water or air past (e.g., small ) simply main- the gills and therefore act as suction pumps. tain shore position and are emersed as a Hemolymph flows through the gills in the consequence of location (deFur et al., 1983). opposite direction from the water or air, By maintaining shore position, small Can- resulting in counter-current gas exchange. cer productus retain contact with seawater. Pressure in the branchial chambers is below Although this seawater is hypoxic, other ambient during forward ventilation, and branchial functions continue and thus CO2 when ventilation is reversed, branchial excretion is maintained (deFur et al., 1983). pressure rises above ambient. The gills are Three species of burrowing mud , located just before the heart in the circu- Upogebia, retreat into their and latory system, thus both perfusion and position themselves at the air-water inter- transmural pressures are low. Ventilatory face to ensure access to water during emer- flow may cease for long periods of time, sion (Hill, 1981). This position may also and such apnea as well as reversals are com- permit access to aerial oxygen when water mon in all species studied so far. Oxygen becomes hypoxic. Grant and McDonald diffuses across a layer of both epithelium (1979) observed that the mud crab Eury- and chitin at the gill, and is transported by panopeus depressus is rarely active on top of the hemolymph to the tissues. Decapods the substrate at low tide, but may remain typically possess the respiratory pigment in burrows, beneath shells and in oyster hemocyanin dissolved in the hemolymph. reefs for protection. Thus, there seem to Hemocyanin is responsible for a large frac- be two types of behavior—remaining in tion of the oxygen transported to the tis- water or as close to it as possible; and sues under a variety of conditions. Tissue remaining active in air to continue feeding, oxygen transport may be altered by changes mating and other activities. Some species in cardiac stroke volume or rate or both in this latter group, e.g., the ghost crab, during periods of increased oxygen demand Ocypode, are considered terrestrial, even (McMahon and Wilkens, 1975; McMahon though they inhabit the upper intertidal etal, 1979). zone. These species represent those which can effectively extract oxygen from air and Responses to emersion maintain or elevate oxygen uptake in air. There are two types of data on ventila- The behavior of decapods during emer- tion during emersion: 1) ventilatory flow sion provides some clue as to the capabil- and 2) scaphognathite rates and activity ities and adaptability of the respiratory sys- patterns. Ventilatory flow rate has been tems to air breathing. A few species, notably measured in both air and water in only fiddler crabs of the genus Uca, migrate three species: (subtidal) between air and water and leave the water (O'Mahoney and Full, 1984; Batterton and voluntarily without any adverse conditions Cameron, 1978), guanhumi forcing them out of the water. This behav- (amphibious) (O'Mahoney and Full, 1984) ior is probably true for Pachygrapsus cras- and lateralis (terrestrial) (Taylor sipes and, to a lesser extent, the mud crab and Spencer-Davies, 1982; O'Mahoney and Panopeus herbsti. It is probably safe to Full, 1984). In the former two species, ven- assume that oxygen supply is sufficient to tilation is considerably lower in air than in meet the demand during emersion in these RESPIRATORY ADAPTATIONS OF INTERTIDAL DECAPODS 117

Heart

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1min 10 sec FIG. 1. Recordings of branchial pressures and heart rate of a small Cancer productus during emersion (A) and in water following reimmersion (B) at 10°C and salinity 33%o. Note that branchial pressures are primarily subambient in both A and B and of much greater magnitude in A. Zero point in A established by briefly removing the catheter from the branchial chamber. In B, the recording begins at the end of a 12 min pause, indicating the zero point for branchial pressures. Taken from deFur and McMahon, 1984a. water, but in Gecarcinus, O'Mahoney and McMahon, 1984a). Several intertidal Full (1984) and Taylor and Spencer-Davies species exhibit a reduction in ventilatory (1982) report conflicting results for the frequency, regardless of the ventilatory change in ventilation in water. There are pattern prior to emersion. This reduction insufficient data to confirm any trend in in frequency is accompanied by a shift in ventilation of intertidal decapods, similar the pattern of scaphognathite activity from to the hypoventilation observed in terres- continuous or periodic to one which is trial vs. aquatic species (see McMahon and intermittent (Fig. 1). Subtidal decapods, on Wilkens, 1983). It is worth noting that there the other hand, exhibit a marked increase is no a priori reason to predict failure of in frequency which is maintained for many the ventilatory mechanism on morpholog- hours and is associated with internal ical grounds because both water and air hypoxia (Table 1). Similar responses occur breathing crabs use the same mechanism. in submerged decapods in hypoxia Ventilatory patterns of all decapods (McMahon, 1988). Unlike hypoxia in water, studied change dramatically during emer- however, high frequency ventilation may sion, and the speed of the response sug- be maintained at very low hemolymph oxy- gests neuronal control (deFur and gen tensions, even if no measurable oxygen 118 PETER L. DEFUR

TABLE 1. Respiratory function of various decapods in air and water.

Mo, water (umol/ PAQ^ water PAO air Species kg-m in) Mo, air (Torr) (Torr) Source Helice crassa 339.2 314.5 Hawkins et al., 1982 Macropthalmus hirtipes 301.7 265.2 Carcinus maenas 37 43 74.9 ± 7.3 18.8 ± 2.0 Taylor and Butler, 1978 73.8 ± 1.9 38.0 ± 1.9 Depledge, 1984 Callinectes sapidus 83 29 O'Mahoney and Full, 1984

112.5 24 deFur et al, 1988 Downloaded from https://academic.oup.com/icb/article/28/1/115/169154 by guest on 23 September 2021 Cardisoma guanhuini 45 49 O'Mahoney and Full, 1984 Gecarcinus lateralis 14 93 O'Mahoney and Full, 1984 Pachygrapsus crassipes 31 69 Burnett and McMahon, 1987 Eurytium albidigitium 19 4 Burnett and McMahon, 1987 Cancer productus large 12.6 3.3 56.6 10 deFur and McMahon, 1984a Cancer productus small 39.3 5.8 59 21.7 deFur and McMahon, 1984a Cancer anthonyi 49 12.6 deFur and McMahon, 1980 Cancer magister 32.3 7.8 deFur and McMahon, 1980 Paguristes turgidus 83.3 25 Burggren and McMahon, 1981 a Pagurus hirsutisculus 30 125 Burggren and McMahon, 1981 a 63.3 Limulus polyphemus 60 7-12 Johansen and Peterson, 1975 10.8 3.9 Mangum et al., 1975 Austropotamobius pallipes 12.13 11.63 33 ± 5 11 ± 1 Taylor and Wheatly, 1980

is being delivered to the tissues (e.g., Cancer of this response. Two sublittoral species, productus, deFur and McMahon, 1984a). large Cancer productus (deFur and McMa- Based on those data, deFur and McMahon hon, 1984a) and C. magister (deFur and (1984a) concluded that the ventilatory McMahon, 1980) are unable to maintain response is mediated or affected by factors measurable branchial pressures in air and other than oxygen alone. Massabuau et al. are also incapable of maintaining oxygen (1984) reached a similar conclusion in uptake or hemolymph pH in air (deFur and describing the CO2 sensitivity of the ven- McMahon, 1980; deFur and McMahon, tilatory drive of crayfish. They concluded 1984a). that the intensity of CO2 stimulation is This intermittent ventilatory behavior is directly related to metabolism and indi- lacking in intertidal crabs which use other rectly related to oxygen level. means to maintain branchial functions. In some species, scaphognathite activity Instead, morphological adaptations permit becomes pulsatile in air and is associated Sesarma reticulatum (Felgenhauer and with an increase in the amplitude of the Abele, 1983) and Helice crassa (Hawkins and branchial pressures (Wolcott, 1976; deFur Jones, 1982) to recirculate water from the and McMahon, 1980; deFur, 1982; Fel- exhalent channel, down the carapace and genhauer and Abele, 1983; deFur and back into the inhalent apertures (Table 2). McMahon, 1984

TABLE 2. Branchial activity and water movement in intertidal crabs in air.

Branchial Water Species pressures uptake Other Source Ocypode quadrata yes yes Wolcott, 1976 Uca pugnax yes yes Felgenhauer and Abele, 1983 Small Cancer productus yes ? deFur and McMahon, 1984a Large C. productus no ? deFur and McMahon, 1984a Sesarma reticulatum no yes recirc Felgenhauer and Abele, 1983 Helice crassa recirc Hawkins and Jones, 1982

Macropthalmus hirtipes ? no recirc Hawkins and Jones, 1982 Downloaded from https://academic.oup.com/icb/article/28/1/115/169154 by guest on 23 September 2021 Panopeus herbsti yes ? deFur, 1983 Carcinus maenas yes ? Taylor and Butler, 1978 deFur and McMahon, 1980 Branchial pressures are subambient and greater than in water. Recirculation (recirc) of branchial water occurs via movement down the front of the carapace. See text for further explanations. intertidal zone, is not able to either recir- Mo2 or ventilation. This reduction in Po2 culate water or develop large subambient necessarily causes a reduction in O2 con- pressures, and decreases Mo2 in air (Hawk- tent as well. The shore crab, Carcinus ins and Jones, 1982; Hawkins^ai, 1982). maenas, an effective air breather, exhibits Thus, in several species, ventilatory adap- a 50% reduction almost immediately upon tations combined with specific behaviors air exposure. Small Cancer productus also permit decapods to survive low tide emer- shows a decrease in PAO2, but this species sion. cannot maintain Mo2 in air (deFur and Measurements of oxygen uptake (Mo2) McMahon, 1984a). Decreased arterial Po2 during emersion in intertidal decapods are is accompanied by an elevation of internal useful for predictive purposes, but only with Pco2. Carcinus maenas, for example, shows knowledge of natural conditions. Measure- an increase in Pco2 of 1.7 (Taylor and But- ments of Mo2 in both air and water are ler, 1978) to 3.5 mm Hg (Truchot, 1975) available for more than a dozen species during 3-4 hr emersion and small C. pro- (Table 1), but only two maintain oxygen ductus elevate Pco2 by about 2.0 mm Hg uptake during emersion. Two of the other within the first hour of emersion (deFur species, Pachygrapsus crassipes, and the her-and McMahon, 1984ft). These results indi- mit crab, Pagurus hirsutisculus, actually ele- cate a gas exchange limitation at the gill, vate Mo2 (the latter was admittedly more or a shunting of hemolymph away from the active in air, elevating oxygen demand; gill. Air breathing decapods also have a Burggren and McMahon, 1981a). Two of higher internal Pco2 (Table 3), indicating the remaining species, Eurytium albidigitum that similar factors influence air breathing and small Cancer productus, occur intertid- in all decapods. ally, remain quiescent in air and reduce There are several explanations for the Mo2 considerably (Table 1). However.small limitation of gas exchange during air C. productus accumulate lactate, indicating breathing by decapod crustaceans in gen- a shortfall of oxygen supply (deFur and eral, and in particular by emersed inter- McMahon, 1984ft), while Eurytium simply tidal species. These include hypoventila- reduces oxygen demand (Burnett and tion in air, a diffusion limitation presented McMahon, 1987). Thus, changes in oxy- by the gills, a smaller surface area available gen uptake must be considered in the con- for gas exchange in air breathing deca- text of oxygen demand, especially for active pods, collapse of the gills, and a perfusion species. limitation. These are discussed below in more detail, but at present it is not possible Gas exchange to clearly identify any one cause as the pri- All the species examined thus far exhibit mary one in most species. Several factors a reduction of arterial hemolymph oxygen may, and probably do, contribute to the tension (Table 1), regardless of changes in limitation of gas exchange in air, as in the 120 PETER L. DEFUR

TABLE 3. Arterial hemolymph oxygen and carbon dioxide tensions in some air breathing decapods.

Species Pcoj (Torr) Po, Source

Gecarcinus ruricola IITO Mileson and Packer, 1986 Gecarcinus lateralts 9.0 Howell e/a/., 1973 11.0 23.0 Burggren and McMahon, 19816 Coenobita brevimanus 9.0 24.0 Burggren and McMahon, 1981* C. clypeatus — 13.7 Burggren and McMahon, 1979 Birqus latro 7.1 27.0 Burggren and McMahon, 198U Ocypode quadrata — 20.0 Burnett, 1979 Downloaded from https://academic.oup.com/icb/article/28/1/115/169154 by guest on 23 September 2021

shore crab, Carcinus maenas. Truchot Total gill area is lower in intertidal than (1975) attributed a respiratory acidosis in in aquatic species and lower still in terres- Carcinus maenas to hypoventilation, but trial crabs (Gray, 1957; Aldridge and Cam- made no direct measurements. However, eron, 1979; Hawkins and Jones, 1982; Taylor and Butler (1978) suggested that Rabalais and Cameron, 1985). Hawkins and the chitin and epithelial layers at the gill Jones (1982) also make the observation that act as a diffusion barrier. Their explana- total gill area is lower in the upper inter- tion for the lack of a diffusion limitation tidal species Helice crassa than in M. hirtipes in water is the high ventilation rate in water. which burrows in mud banks in lower As pointed out above, there are few data intertidal areas. This reduction has been on ventilatory flow in air and water for considered an to reduce evap- intertidal species, and it is not possible to orative water loss, but is also a possible lim- resolve the difference without additional itation of gas diffusion. data. The possible collapse of gill lamellae in There has been no systematic survey of air is another factor that bears serious con- the diffusion path length at the respiratory sideration because it has been cited fre- surface in decapods, so the data here are quently yet there are no data available on only from the few available representa- this phenomenon. The gill lamellae of tives. The respiratory surface is not of uni- decapod crustaceans are so close together, form thickness in most species, especially even in the land crab Gecarcinus (Copeland, those which osmoregulate. Barra el al. 1968), that capillary conduction, not active (1983) described the ultrastructure of the convection, of water between the lamellae gills of the , Eriocheir has been suggested or assumed as the prime sinensis and document great variation in mechanism. Land crabs have morpholog- chitin and epithelial layers among and ical modifications to maintain spacing and within individual platelets. Anterior gills prevent surface adherence (Cameron, tend to have a 3-5 jum diffusion distance 1981; Maetzold and deFur, 1984). Without but in posterior gills where ionregulatory such modifications, gills of other species, tissue is located, the epithelium may be 10 including intertidal ones, probably do nm thick. Similar trends are true in the adhere together in air, greatly reducing subtidal crab, Callinectes sapidus (Copeland the surface area available for diffusion. and Fitzjarrel, 1968). The intertidal shore Johnson and Uglow (1985) noted that Car- crab, Carcinus maenas, also a portunid, has cinus maenas does have such modifications. a diffusion path length of 6 jim (Taylor and deFur et al. (1988) noted that the gills of Butler, 1978), and the gills are more uni- blue crabs were tightly adhered together form than in Callinectes, with only thin epi- during emersion. Obvious clumping did thelium throughout (Pequeux et al., 1984). occur after several hours, and this change Some terrestrial crabs may indeed have may actually increase surface area by thicker epithelial and chitin layers (Cope- exposing an entire lamellar surface between land, 1968; Maetzold and deFur, 1984), clumps. but the differences, based on published deFur and McMahon (1984a) reported data, seem small and insufficient to account a bradycardia and decrease in calculated for a large reduction in diffusion. cardiac output in small Cancer productus RESPIRATORY ADAPTATIONS OF INTERTIDAL DECAPODS 121

during emersion, and concluded that oxy- r-mn < •— —o— ^-—•— gen uptake was at least partially perfusion ami limited. Another perfusion limitation

would be shunting of hemolymph flow away mocy 3 from the gills. Johnson (1980) described c c the structure of the gill of Callinectes as Hei Pao

of " f / having capillaries which carried hemo- c 60 lymph across the face of the lamellae. o Assuming a perfusion pressure of 2.0 cm +-»

ra Downloaded from https://academic.oup.com/icb/article/28/1/115/169154 by guest on 23 September 2021 H2O, and a branchial pressure of 2.0 cm (_ H2O below ambient, the transmural pres- $40 sure would be only 4.0 cm H O. A slight 2 c 0) decrease in this pressure could reduce cap- D) illary radius considerably and elevate bran- K 20 chial resistance to hemolymph flow. Since O o 2 flow is proportional to the radius to the o -f° fourth power, flow through the gill could / I I I 11 1 easily decline dramatically. I 2I0 I 40I I 60 80 140 PCX, (torr) Hemocyanin function FIG. 2. Oxygen equilibrium curves for the hemo- At the low arterial oxygen tensions cyanin of small Cancer productus at pHa = 7.98 and occurring during emersion, the oxygen pHv = 7.90 at 10°C and acclimated to 33%o salinity water. The lowering of pHv shifts the curve to the affinity of the respiratory pigment, hemo- right, with a reduction in hemocyanin bound oxygen. cyanin, must be sufficiently high that the Taken from deFur et al, 1983. pigment becomes saturated in passage through the gills. Concomitant elevation of CO2 provokes an acidosis which lowers cooperativity nor the Bohr shift are sig- oxygen affinity due to the Bohr shift. This nificantly different in water vs. air or bi- situation occurs in several intertidal species, modal tropical crabs. Few temperate zone including the shore crab, Carcinus (Taylor species have been studied, but at least Car- and Butler, 1978) an effective air breather, cinus maenas (Taylor and Butler, 1978) and and small Cancer productus which cannot Cancer productus (deFur and McMahon, maintain Mo2 (deFur and McMahon, 1984a) fit this pattern. Thus, under the 1984a). Both species experience internal hypoxic conditions prevailing during hypoxia and hemolymph acidosis. How- emersion (Table 1) and in most air breath- ever, venous pH is lower than pHa and ers (Table 3), hemocyanin can still be fully venous Po2 falls, enhancing oxygen deliv- saturated at gill. The higher hemocyanin ery to the tissues (Fig. 2). Mangum (1982) oxygen affinity represents an adaptation to reported that oxygen affinity of hemocy- the reduced oxygen tensions associated anin in tropical decapods is higher in air with air breathing. breathing and bimodal species (P50 = 10.7 ±1.6 mm Hg, n = 13) than in water Circulatory function breathers (P50 = 18.7 ± 2.7 mm Hg, n = Lower arterial hemolymph oxygen ten- 14), although Young (1972) had come to sions during emersion have quantitative the opposite conclusion ten years earlier. consequences with regard to tissue oxygen Both studies may provide only general- supply. Based on the Fick equation, Mq = izations which must be re-evaluated in.light 2 Vb (CAO2-CVO2), in order to maintain Mo2 of recent information about modulators of at pre-emersion levels, an animal must be hemocyanin oxygen affinity, but the trend able to increase blood flow to the tissues, noted by Mangum (1982) is consistent with Vb, or decrease oxygen saturation and the latest work (Morris and Bridges, 1985) hence CvO2 of venous hemolymph. Few, if and is probably still valid because the con- any, species elevate heart rate during ditions were constant and comparable. emersion, and there is only one report of According to Mangum (1982), neither an elevated cardiac stroke volume {Card- 122 PETER L. DEFUR

nus maenas: Taylor and Butler, 1978). A /., 1975). Gas exchange, how- decrease in CvO2 is easier to explain in light ever, remains limited as demonstrated by of the other events, and occurs in Cancer the fall in oxygen uptake reported by Man- productus (deFur and McMahon, 1984a) and gum et al. (1975; Table 1). Under these Carcinus maenas (Taylor and Butler, 1978). conditions, cardiac output, calculated from Intertidal and subtidal decapods exhibit the Fick equation, decreases by 2/s, about a bradycardia when exposed to air and the the same decrease as oxygen uptake (Man- land crab, Gecarcinus lateralis, does so in gum et al., 1975). water (O'Mahoney-Damon, 1984). It is not

Responses of the crayfish, Austropotamo- Downloaded from https://academic.oup.com/icb/article/28/1/115/169154 by guest on 23 September 2021 clear what other circulatory adjustments to biuspallipes (Taylor and Wheatly, 1980), to emersion occur, but internal pressures must short term air exposure, are comparable be maintained to oppose the loss of support to those described above for intertidal crabs provided by water. The terrestrial deca- (Table 1). A. pallipes maintains oxygen pods (Burggren et ai, uptake in air, hemolymph oxygen is low 1985) and Gecarcinus ruricola (Maetzold and and accompanied by a bradycardia. There deFur, 1984) have much higher internal are two real departures from the patterns pressures which also vary considerably with described above: there is an increase in sca- branchial activity. Taylor and Greenaway phognathite frequency in air; and Taylor (1984) demonstrated that in one land crab and Wheatly (1980) measured low hemo- hemolymph shunted from the gills to the lymph oxygen tensions in both water and lungs, and similar processes may be part of air. It is not clear if there is any significance the adjustments of intertidal species. to the elevated scaphognathite rates in air.

Comparison with other groups Conclusions The horseshoe crab, though not a crus- There are few obvious respiratory adap- tacean, is intertidal during part of its life tations of intertidal decapods, especially for history, when mating and laying in maintenance of oxygen uptake in air. Sev- the spring. At least three studies of air eral species exhibit adaptations to maintain exposure in Limulus polyphemus provide access to or flow of water in the branchial further evidence of the limitation of gas chamber. This water may serve as a source transport and the adaptability of this of oxygen for some species, but it is more hemocyanin. Johansen and Petersen (1975) likely that this branchial water is important emersed Limulus for periods of up to 48 for carbon dioxide excretion, ion regula- hr and measured hemolymph gases and pH. tion and acid-base balance. Burnett (1988) Both arterial and venous Po2 declined rap- also emphasizes the importance of bran- idly during the first hour of emersion chial water for active process in acid-base (Table 1), and this decrease was accom- balance of intertidal crabs. Availability of panied by elevation of Pco2 from 2.9 to at water is critical for gas exchange at the gill, least 6.2 mm Hg. In another study, Red- because even a slight flow of water between mond et al. (1982) reported that heart rate lamellae will permit use of that surface. and blood pressure decrease within the first With no water flow between the lamellae, few minutes of emersion. Prolonged emer- the adhering of the gill lamellae will cer- sion results in an elevation of arterial Po2, tainly make that surface unavailable for gas but not to pre-emersion levels, and Pco2 exchange. The rapid and profound alter- continues to rise (Johansen and Petersen, ation of respiratory activity in air is prob- 1975). The hemocyanin of Limulus has a ably neurally mediated. A higher oxygen reverse Bohr shift which is highly adaptive affinity of hemocyanin of intertidal crabs under conditions of air exposure because is adaptive, but there is no reason to sup- a respiratory acidosis increases oxygen pose that the change was not first associ- affinity, permitting higher oxygen satura- ated with hypoxia in water (see McMahon, tion at low Po2 at the gills. The net effect 1988). Structural modifications of the is that 90% of the oxygen delivered to the branchial chamber and of the outer surface tissues is transported by the hemocyanin of the carapace are certainly the most pro- RESPIRATORY ADAPTATIONS OF INTERTIDAL DECAPODS 123 found adaptations demonstrated in this deFur, P. L. and B. R. McMahon. 1984a. Physiolog- group of animals. ical compensation to short term air exposure in Red Rock crabs, Cancer productus Randall, from littoral and sublittoral habitats. I. Oxygen uptake REFERENCES and transport. 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