Endogenous rhythm, light and salinity effects on postlarval brown shrimp Penaeus aztecus Ives recruitment to estuaries

J. Exp. Mar. Biol. Ecol., 154 (1991) 17%189 © 1991 Elsevier Science Publishers B.V. All rights reserved 0022-0981/91/$03.50

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JEMBE 01690

Endogenous rhythm, light and salinity effects on postlarval brown shrimp Penaeus aztecus Ives recruitment to estuaries Thomas R. Matthews J, William W. Schroeder I and Don E. Steams 2 Marine Science Program, University of Alabama, Dauphin Island, Alabama, USA; ZDepartment of Biology, Rutgers University, Camden, New Jersey, USA (Received 16 August 1991; revision received 5 August 1991; accepted 4 September 1991) Abstract: The interaction between endogenous rhythms, light and salinity changes on postlarval brown

shrimp Penaeus aztecus Ires activity levels was examined under laboratory conditions. Understanding how these factors interact will help us better understand estuarine recruitment and retention. Postlarvae have strong circadian and occasional circatidal activity rhythms. The postlarvae respond to salinity increases and light level decreases by increasing swimming activity. The postlarvae decrease swimming activity in response to decreases in salinity and increases in light. These changes in activity occur only during dark/nocturnal conditions. Temporally selective activity in the presence of different environmental signals attests to the plasticity of a postlarva's response to environmental signals and provides a mechanism for estuarine immigration. The presence of a response hierarchy to environmental signals may also help account for the ability of postlarval penaeids to immigrate into estuaries with different hydroperiods and salinity regimes. Key words: Endogenous rhythm; Estuarine recruitment; Penaeus aztecus; Postlarva; Tidal behavior

INTRODUCTION

A critical part of the life cycle of brown shrimp Penaeus aztecus Ives is the migration of the postlarvae from offshore spawning grounds to inshore nursery areas (Christmas et al., 1966; White & Boudreaux, 1977; Van Lopik et al., 1979). Failure to reach the nursery will severely limit the growth and survival of postlarvae (Costello & Allen, 1960; Baxter & Renfro, 1967; Minello et al., 1989). As zooplankters capable of vertical migration, postlarvae are capable of selectively entering shoreward currents, thur enhancing estuarine recruitment ((3urney, 1924; Foxon, 1934). The mechanisms and cues used to facilitate this migration vary between species and locations Light i:~tensity and salinity concentration gradients are two factors known to be important in estuarine recruitment of postlarvae (Hughes, 1969, 1972; Macias-Regalado et al., 1982; Forbes & Benfield, 1986). Manipulations of the presence or absence of light and increasing or Correspondence address: T. R. Matthews, Florida Marine Research Institute, 13365 Overseas Highway, Marathon, FL 33050, USA. Contribution 163 of Aquatic Biology Program, University of Alabama; Contribution 194 of Marine Environmental Sciences Consortium.

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decreasing salinity concentrations in the laboratory will identify how these factors interact to control the timing of postlarval immigration to estuaries. The currents that transport these planktonic larvae to coastal waters may be available on a regular cycle, like the tides, or they may be aperiodic. Aperiodic currents may vary in duration and intensity depending on the mechanism driving them (Dayton & Tegner, 1984; Johnson et al., 1984; Schroeder & Wiseman, 1986; Tegner, 1986; Epifanio, 1987; Gacic et al., 1987; Shanks & Wright, 1987; Wiseman et al., 1988). The ability to utilize currents is often dependent on the biology and behavior of the organism. Vertical migration, either entirely within the water column or from the benthos to the water column, is one of the most prevalent mechanisms allowing differential use of currents to maintain a position in (Stubblefield et al., 1984; Cronin & Forward, 1986; Kimmerer & McKinnon, 1987) or be transported from (Henderson, 1987) an area. Among the penaeids, the magnitude of the vertical migration seems to be dependent on the developmental stage. Postlarval stages tend to migrate deeper during the day than the protozoeal or mysis stages (Temple & Fisher, 1965; Rothlisberg, 1982). The more pronounced vertical migrations of the postlarvae probably allow this stage to utilize specific currents to a greater degree than the younger stages. Activity cycles for many penaeids have diel and tidally mediated frequency components (Dakin, 1938; Racek, 1957, 1959; Fuss & Ogren, 1966); however, the extent to which the diel or tidal factors affect activity levels vary depending on the hydrographic characteristics of the bay itself (Tabb et al., 1962; Beardsley, 1970; Hughes, 1972). Recent studies provide evidence that immigrating postlarvae utilize currents for transport into estuaries (Youngbluth, 1980; Macias-Regalado et al., 1982; Rothlisberg, 1982; Forbes & Benfield, 1986), but there is no consensus on which signals the postlarvae specifically respond to within a current. Experimental evidence suggests that postlarvae respond to factors'such as changes in salinity (Hughes, 1969) and hydrostatic pressure (Forbes & Benfield, 1986) which covary with the tide, instead of responding to currents directly. However, salinities fluctuate in coastal embayments and may even become hypersaline in estuaries with high evaporation. Penn ( 1975) observed postlarval Penaeus latisulcatus (Kishinouye) moving into Shark Bay, Australia while it was hypersaline; salinity increases are not associated with flood tides in this situation. Diel and tidal signals may also entrain endogenous rhythms. These circadian and circatidal activity rhythms in penaeids (Wickham, 1967; Hughes, 1972; Subrahmanyam, 1976)may have a role in predator avoidance and transport into the estuary. A diel rhythmic behavior allows postlarvae to limit their exposure to swimming visual predators by entering the water column only when light levels are low enough to minimize detection. Tidally rhythmic behavior may aid in estuarine recruitment and retention. However, endogenous rhythms can become detrimental if aperiodic events have a major impact on the environment. Because estuaries are subject to rapid fluctuations due to the weather, tidal signals can be masked or reversed. Postlarvae capable of responding to these aperiodic signals by overriding previously entrained endogenous rhythms may better control their horizontal advection.

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This study will examine the effect changes in light level and salinity concentration have on freshly captured postlarvae with distinct activity rhythms. The postlarvae's ability to adjust their behavior and optimize recruitment into estuaries in response to changing environmental conditions will be discussed.

METHODS

All experimental postlarval P. aztecus were collected in 500-#m surface-towed plankton nets in Mobile Bay, Alabama, from May to November 1987. The postlarvae were collected at night and held in the dark until dawn when individuals between 10 and 13 mm were collected for later experimentation. The postlarvae used in the 16-18 September experiment were inadvertently exposed to light prior to dawn. Experimental animals were held under constant dim red light conditions at least 1 h prior to experimentation and fed a diet of finely ground fresh shrimp ad libitum. Species identification of postlarval penaeids requires microscopic examination, so species identification was determined after the experiments were completed. Those tests which included more than one white shrimp Penaeus setiferus (Linnaeus) were discarded. Identification of the postlarvae followed the method developed by Zimmerman & Prior (1987). Endogenous activity rhythms were examined using two approaches. The first set of experiments involved a modification ofthe free-running procedure described by Cronin & Forward (1979). Groups of 10 postlarvae were placed in a transparent 1-1, 7-cm diameter Plexiglas cylinder within 4 h of capture. Observations took place hourly for 50 h under constant dark conditions. A dim red light was used to illuminate the cylinders during the 5-s observation period each hour. Percent activity was determined by dividing the number ofpostlarvae actively swimming in the water column by the total number of postlarvae in the cylinder. Animals in contact with the edges of the cylinder were not included in the activity level calculations. Three ~.xperiments were carried out beginning 18 May, 16 September and 30 September 1987 utilizh~g 4C,, 100 and 80 animals, respectively. The second set of endogenous rhythnl experiments involved making seven observations at 10-min intervals on groups of 10 postlarvae under different combinations of day (1000-1500 CST) or night (2000-2400 CST) and light (100 #E. m - 2. s - ~) or dark ( < 1 # E . m - 2 . s - ~) conditions. Activity levels were determined as in the free-running experiments. For each test, seven observations were averaged to calculate a mean activity level. After log-transformation to meet Bartlett's homogeneity of variances test, a two-way ANOVA was used to examine the interaction between the main effects of day/night and light/dark on mean activity level. A Student-Newman-Keuls (SNK)test for nonsignificance (P > 0.05) among groups was used to identify different cells (Sokal & Rohlf, 1981). Additional experiments to quantify the effect changing salinity concentrations and alterations of the presence or absence of light have on postlarval activity levels were

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conducted under four combinations of clay/night and light/dark conditions. The salinity concentration in each chamber was increased or decreased in four replicate trials from 10 to 15%oor 10 to 5%o in each test chamber by adding 15 or 5%o seawater solution over a 1-h period. A control chamber was designed to simulate the water currents in the experimental chambers by adding isohaline seawater. These salinity concentrations are comparable to those observed in the field (Matthews, 1988). Slightly different laboratory setups were required for each salinity alteration experiment. The hyposaline water entered near the bottom of the observation tube, allowing mixing to occur as the less dense water rose to the surface. The hypersaline water entered at the top ofthe chamber and also mixed evenly as it sank. The 5%o salinity changes took place over a 1-h period. As in the earlier experiments, seven observations at 10-min intervals were used to calculate a mean activity level during the salinity change. Altering the presence or absence of light was done by instantly turning on or off the light. No control chambers were used due to the inability to simultaneously observe both light and dark conditions. Instead a control was calculated by averaging the seven observations made prior to the light level change. Two separate two-way ANOVAs were used to analyze the manipulative laboratory experiments. The first ANOVA examined the interaction between the main effects of test condition (day/light, day/dark, night/light, and night/dark) and salinity change (increasing, decreasing, and two controls). The two control tests were reported separately, because of the difference in the observation chambers. The second ANOVA examined the interaction between the main effects of test condition (day or night) and light level change (light-dark or dark-light). Both manipulative laboratory tests met Bartlett's test for homogeneity of variance, although the salinity change experiment required log-transformation. An SNK test for nonsignificance among groups was performed for each ANOVA.

RESULTS

The free-running endogenous experiments strongly suggest that postlarvae increase their activity level at night in the absence of any external cue (Fig. 1). There were distinct and immediate activity increases at dusk, 38 and 34~ during the 18-20 May test (Fig. la), 19 and 28°o during the 16-18 September test (Fig. lb), and 29 and 15~ during the 30 September to 2 October test (Fig. lc). The decrease in activity in the predawn hours of the 18-20 May and 30 September to 2 October tests also suggests that there is a circadian rhythm involved with this behavior. The normal predawn decrease in activity during the 16-18 September test (Fig. lb) may have been delayed due to an experimental artifact caused by sorting the postlarvae at night under light conditions. The sorting procedure occurred after dawn in the other tests and did not seem to affect the activity rhythms. The relationship between the flood and ebb periods of the tides and postlarval activity

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levels is difficult to distinguish (Fig. 1). The difficulty in distinguishing circatidal rhythms lies in part with the tendency of the postlarvae to become active every evening independent of the direction of tidal flow. This delays any postlarval activity change due to tidal effects until after the dusk induced activity, as can be observed in both night portions of the 18-20 May test (Fig. la). During the 18-20 May experiment, the initial nocturnal activity is suppressed by the ebb tide conditions until a few hours before dawn. As the tide turned, the activity level increased to near-dusk levels. These results suggest a tidal rhythm at night. During the 16-18 September experiment (Fig. lb), flood tide occurred during the nocturnal period, so differentiation between circadian and circatidal

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T.R. M A T T H E W S ET AL.

rhythms was impossible. The relationship between tidal phase and activity level is 180 ° out of phase during the 30 September to 2 October test (Fig. lc). Examination of the circadian rhythm using ANOVA techniques indicated that the nocturnal increases in activity were due to an internal timing cue and not simply a direct response to light. Both night and dark conditions were required in the laboratory for the increased activity level to be expressed (Table I). Dark conditions during the day TABLE ! Postlarvai activity levels ( ~ ) + SE in response to time of day and light level (n - 20 groups of 10 animals). Superscripted values do not differ significantly by S N K comparison (P > 0.05).

Light

Day

Night

20. ! __ 6. ! ~

20.0 + 8.0 a n - 20 55.4 + 14.8 b n = 20

n

Dark

Time of day Light level Time of day x light level Error

=

20

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df

F

P

6. i 66 4.033 4.886 ! 7.106

1 1 1 76

27.396 17.919 21.707

< 0.001 < 0.001 <0.001

are not sufficient to significantly change the activity level from that normally expressed during day/light conditions. The experiment also showed the presence of light during night conditions inhibited activity levels to daxtime levels. TxBII

il

Change in postlarval activity levels (~/o) +- SE in response to salinity changes (n = 4 groups of 10 animals). Superscripted values do not differ significantly by S N K comparison (P > 0.05).

Increase Decrease Control (for increase) Control (for decrease)

Day/Light

Day/Dark

Night/Light

1.5 + 8.2 b 0.25 + 3.4 b 4.0 + 4.1 b

1.5 + 3.7 b - 0 . 7 5 + 0.11 b 3.5 + 3.1 b

2.5 + 2.6 b !.5 + 1.7 b - 0 . 5 + 6.0 b

1 0 ± 1.4 b

1.25 + 4.7 b

5.25 + 2.6 b

Test conditions Salinity change Test conditions x salinity change Error

Night/Dark 15.5 + 13.8 a - 2 4 . 2 5 + 6.9 c

- 0 . 7 5 _+ 3.9 b 1.25 _.+ 3.1 b

ss

df

F

P

162.9 1339.7 2183.1 1738.3

3 3 9 48

1.5 12.331 6.698

NS < 0.001 <0.001

FACTORS IN BROWN SHRIMP RECRUITMENT

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A two-way ANOVA between test condition and salinity change revealed a significant (P < 0.001) interaction (Table If). The SNK procedure identified the night/dark increasing and decreasing salinity cells as different (P > 0.05). An increase in salinity caused an increase in activity (Fig. 2a), while a decrease in salinity caused a decrease in activity (Fig. 2b). ,~ 30 min is required before the salinity increases or decreases have a visible effect on the swimming activity of the postlarvae.

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T.R. MATTHE,VS ET AL.

A significant interaction exists between test conditions and light change (P < 0.001, Table III). The SNK procedure (P > 0.05)determined that the change from dark to light conditions at night and the change from light to dark conditions at night are significantly different from each other and from both effects tested during the day. Thus, during

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F A C T O R S IN B R O W N S H R I M P R E C R U I T M E N T

185

TABLE III Changes in postlarval activity levels ( ~ ) + SE in response to light level changes (n = 4 groups of 10 animals). Superscripted values do not differ significantly by S N K comparison (P > 0.05).

Light - dark Dark - light

Test conditions Light change Test conditions x light change Error

Day

Night

3.25 + 5.2 b n =4 3.75 + 7.0 b n = 4

15.5 + 2.6" n =4 - 2 0 . 3 + 5.4 c n = 4

ss

df

F

P

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1 1 1 12

4.861 47.632 45.023

0.048 <0.001 < 0.001

nocturnal conditions, increased light elicits a decrease in activity (Fig. 3a) and decreased light elicits an increase in activity (Fig. 3b). Activity increases associated with decreasing light levels are delayed for approximately the same length of time as activity increases when salinity is altered (30 min). The decrease in activity associated with light level increases is immediate. DISCUSSION

A hierarchy seems to exist between circadian, circatidal and direct response to stimuli. Postlarvae are most active at night (possibly an evolved response to visual predation). Because day/night cycles are regular and predictable, there has been strong entrainment and hence strong endogenous rhythms with peak activity at night. When predictable tidal cues are present an endogenous tidal rhythm may be entrained, so that the animals move upward (and upstream) during nocturnal flooding and downward to the sediment during nocturnal ebbing tides. Decreases in salinity can cause decreases in activity overriding circatidally entrained rhythms just as increases in salinity can enhance activity. When strong, predictable tidal cues are not available (e.g., during neap tides or aperiodic fresh water flooding), such direct responses to salinity change ensure estuarine retention. Postlarval brown shrimp appear to have strong circadian and occasional circatidal activity rhythms. Spontaneous dusk activity peaks are evident in all free-running experiments. Dusk activity peaks may be a unique feature associated with diurnal tides. Since a nocturnal flood tide may not occur for several consecutive days, a mechanism is required to insure that the postlarvae have the opportunity to forage every day even if

186

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foraging could displace postlarvae from the estuary. In semidiurnal tidal areas, nocturnal increases in activity often coincide with flood tides independent of the time of night (Hughes, 1972), thus allowing retention in the estuary while feeding. This brief activity period has also been seen in Penaeus plebejus, which limits its nocturnal activity to only the first 3 h of a flood tide (Young & Carpenter, 1977). Penaeus duorarum from the Florida Everglades are also abundant in the water column for only a few hours during the strongest flood tides (Roessler & Rehrer, 1971). This limited use of a tidal current may also reflect the time required for the shrimp to obtain adequate food, although there is no direct evidence to substantiate this. The evidence for a circatidal rhythm is mixed. This finding may also be a result of the natural fluctuation between diurnal and semidiurnal tides in this system (Marmer, 1954). Because of the interruption of the diurnal tide every 2wk, a period of reentrainment to the tidal cycle would be expected. Hughes (1972)estimated such a reentrainment period to be ~ 3 days, but 3 days of exposure to diurnal tide conditions were not sufficient to develop a tidally rhythmic behavior in the 30 September to 2 October test. This resu '~ might be due to the lack of a clear timing cue; if indeed the Zeitgeber is salinity change, then any nontidal salinity fluctuations would interrupt the entrainment process. Field samples in a low-tidally influenced area in Mobile Bay have postlarval activity levels similar to the 30 September to 2 October free-running experiment (Matthews, 1988); this finding suggests that changes in activity during the freerunning experiment are real and related to daily light level cycles. Endogenous rhythms are beneficial to postlarvae because the rhythms provide a mechanism for the shrimp to utilize tides more effectively. The postlarvae are not dependent on daily salinity or a hydrostatic cue, which may only be evident several hours after the tide has turned. Ifa mechanism exists that allows postlarvae to anticipate tidal changes, postlarvae can time their movements into the water column and maximize their advection into estuaries. An endogenous tidal rhythm overlying a nocturnal activity cycle may serve this function. In highly variable estuarine environments, postlarvae must also be able to respond directly to unfavorable conditions. The decreased activity associated with decreased salinities demonstrates how postlarvae ensure estuarine retention during ebb tide or aperiodic seaward currents. Observations of freshly captured postlarvae under all combinations of day/night and light/dark conditions suggest that postlarvae are primarily active at night under dark conditions. Darkened daytime conditions are not sufficient to increase activity. This finding is in direct contradiction to field results from Port Aransas, Texas, which indicate that postlarval brown shrimp are more active during the day if there is cloud cover or high turbidity (Duronslet et al., 1972). The postlarvae's depressed activity at night in the presence of light may be due to light inhibition of swimming activity. The timing of the night/dark test, 2000-2400 CST, fell within the dusk activity peak which overrides any tidal effect. Postlarvae responded directly to salinity signals in the laboratory only during night/dark conditions. Specifically, significant activity increases occurred only during

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salinity increases under night/dark conditions. Significant activity decreases occurred only during salinity decreases under these conditions. Salinity changes did not affect postlarvae that were not predisposed (due to an endogenous rhythm) to be active at that time. By increasing or decreasing their activity in association with respective increases or decreases in salinity, postlarvae should be transported to and retained in highly variable coastal areas more efficiently than would be possible utilizing endogenous rhythms alone. Hughes (1969) also tested the effect of salinity changes on postlarval activity, but his results varied considerably, possibly due to endogenous rhythms dictating when a salinity signal will cause a reaction. Postlarvae may respond to several tidal signals. There is little doubt that increasing salinity results in increased postlarval activity in many situations, but this effect would be detrimental to recruitment into hypersaline lagoons such as Laguna Madre in Texas (Gunter, 1950)or Shark River in Australia (Slack-Smith, 1967), or any other situation where evaporation is greater than freshwater input. Since flood tides may not always be associated with salinity increases, successful recruitment might depend on recognizing other tidal cues. Two such cues are hydrostatic pressure and current speed (Heinisch & Wiese, 1987), both can elicit increases in activity. The ability to respond to several different tidal cues attests to the plasticity of postlarval sensory mechanisms to respond to a number of cues in a fashion that will allow the shrimp to be transported into an estuarine environment. It remains to be tested if these other environmental ~J~.a.o-:--^".., ~'" into some type of response hierarchy, or if there is intraspecific variability in larval behavior and recruitment between different estuaries. ACKNOWLEDGMENTS

This research was supported by the U S Department of Commerce, National Oceanic and Atmospheric Administration, National Ocean Service, Office of Ocean and Coastal Resource Management, Marine and Estuarine Management Division under Grant NA86AA-D-CZ017, Office of Sea Grant (Mississippi-Alabama Sea Grant Consortium) under Grant NA85AA-D-SG005 (Project 3/O-16 and the Marine Environmental Sciences Consortium of Alabama. This research could not have been completed without the invaluable assistance of M. Lanoutte, J. Valentine, P. James, D. Nadeau and M. Wilson. REFERENCES Baxter, K. N. & W.C. Renfro, 1967. Seasonal occurrence and size d~stributlon ofpostlarval brown and white shrimp near Galveston, Texas, with notes on species identification. F~sh. Bull., Vol. 66, pp. 149-158 Beardsley, G.L., 1970. Distribution of migrating juvenile pink shrimp, Penaeus duorarum duorarum Burkenroad. Biol. Bull., Vol. 136, pp. 43-53. Christmas, J.Y., G. Gunter & P. Musgrave, 1966 Studies on annual abundance of postlarval penaeld shrimp in the estuarine waters of Mississippi as related to subsequent commercial catches. GulfRes. Rep., Vol. 2, pp. I 17-212.

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