feeding, and social behavior in larval American shad, Alosa sapidissima. Rep- licated prey-density treatments of 1,000, 500, and 0 Artemia nauplifliter and.
0 Munksnaard 1996 CoovriPht ',
Ecology of Freshwater Fish 1996: 5: 163-168 Printed in 1>enmurk -All rights reserved
ECOLOGY OF FRESHWATER FISH 1SSN 0906-6691
Behavioral changes associated with suboptimal prey densities for larval American shad Ross RM, Johnson JH, Bennett RM, Dropkin DS. Behavioral changes
associated with suboptimal prey densities for larval American shad. Ecology of Freshwater Fish 1996: 5: 163-168. 0Munksgaard, 1996 Abstract - Laboratory studies were conducted to determine the effects of suboptimal prey density and length of prey-deprivation period on swimming, feeding, and social behavior in larval American shad, Alosa sapidissima. Replicated prey-density treatments of 1,000, 500, and 0 Artemia nauplifliter and deprivation periods of 0,2, and 4 days were established for an 8-day period. The duration or frequency of 11 behavior patterns was quantified with an event recorder during the experiment. Exposure to suboptimal prey densities affected three categories of larval behavior: swimming activities (pivot and dart), interaction with other larvae (escape or avoid), and stereotypical feeding responses (sigmoid and lunge). Location of a food patch, simulated by the sudden introduction of prey to aquaria, affected the frequency of feeding responses more than other categories of behavior. The patch model was supported as a foraging strategy in larvae. The ontogeny of prey deprivation was evidenced primarily by changes in swimming activity (reduced pivot and dart frequencies), though feeding responses (particularly fixate) were also diminished. Deprivation-induced loss of pivot and fixate was an irreversible, pathological effect of starvation. Deprivation also resulted in greater vertical orientation (head up, 42") of larvae than non-deprived larvae (21-29"). These changes in behavior may result in less effective escape from predators, location of food patches, or pursuit and capture of prey items in riverine habitats.
R. M. Ross, J. H. Johnson, R. M. Bennett, D. S. Dropkin National Biological Survey, Research and Development Laboratory, Wellsboro, Pennsylvania 16901, USA
Key words: Alma sapidissima; American shad;
food patch; foraging behavior; larval fish; prey density R. M. Ross, National Biological Survey, Research and Development Laboratory, Rural Delivery #4, Box 63, Wellsboro, Pennsylvania 16901, USA Accepted for publication October 5, 1995
Un resumen en espaiiol se incluye detrais del texto principal de este articulo.
Introduction The principal causes of mortality in larval fishes, marine or freshwater, are generally thought to be starvation and predation (May 1974; Blaxter & Hunter 1982). Some evidence points to an interaction between the two factors whereby starved or underfed larvae may be more susceptible to predation (Blaxter & Hunter 1982; Neilson et al. 1986; Rice, Crowder, & Binkowski 1987). Much of the interest in starvation as a significant source of natural mortality in pelagic larval fishes was generated by observed natural prey densities well below those shown to promote adequate growth and survival in laboratory studies (Lasker 1975; Hunter 1980; Werner & Blaxter 1980).
The mechanisms by which starvation or food deprivation leads to reduced growth or survival have been studied at several levels of organization, from the molecular to the ecosystem. Changes in body chemistry, including water (increase), triglycerides (decrease), nitrogen (decrease) and ash (increase), were demonstrated by Ehrlich (1974) and Navarro & Sargent (1992). Histological (gut and liver atrophy) and gross morphological (pectoral angle and relative eye-head height) changes were described by Ehrlich, Blaxter & Pemberton (1976). Search or foraging strategies for individuals were modeled and applied to larval fishes successfully (Stephens & Krebs 1986; Browman & O'Brien 1992). Community ecological determinants of larval survival related to prey distribution or abundance
163
Ross et al. (e.g. prey patches in Owens 1981 or zooplankton density in Welker, Pierce & Wahl 1994) and ecosystem physical factors such as winds and currents that determine drift and recruitment (Stevenson 1962; Checkley et al. 1988) have also been shown. Few behavioral mechanisms associated with starvation have been elucidated. Some evidence suggests that general activity or vertical migratory activity falls in starved larvae of several species (Lawrence 1972; Blaxter & Ehrlich 1974; Skiftesvik & Huse 1987). A head-down position in starving herring (Clupea harengus Linnaeus) larvae (Ehrlich et al. 1976), due to expended cephalic lipid stores, may prevent normal foraging behavior. Changes in discrete behavior patterns associated with variable prey densities or starvation periods have not been quantified, however. American shad (Alosa sapidissima Wilson) are anadromous clupeids whose larvae must survive upstream riverine environments. Small crustacean invertebrate prey are often the major food of larvae (Crecco & Blake 1983), but these prey are often depauperate in such habitats (Hynes 1972). Endogenous (yolk-sac) nutrition in American shad larvae ends 3-5 days after hatching. Consequently, prey availability and resistance to starvation are especially important determinants of larval survival for this species (Johnson & Dropkin 1995). The objectives of this study were to determine changes in larval shad behavior (1) at suboptimal prey densities typical of upper riverine environments and (2) after varied prey-deprivation periods. We relate these findings to elements of foraging theory in a patchy environment.
Methods In the first (prey density) experiment, we placed 18day-old (post hatch) American shad larvae (length 10-15 mm) from the VanDyke Fish Hatchery (Pennsylvania Fish Commission) in nine 20-liter aquaria at a density of eight IarvaeAiter, the same density used by Werner & Blaxter (1980). Water temperature was maintained at 20°C with a small aeration-induced current producing little turbulence. Following a 24-h acclimation period with unlimited access to prey, dead larvae were replaced and prey treatments initiated. Previous studies of larval hemng indicated a growth or survival threshold prey density of 100300 brine shrimp (Artemia sp.)Aiter (Werner & Blaxter 1980). Therefore we broadly bracketed this range (and compensated upward since we started with older larvae) with an experimental design of three prey densities of Artemia nauplii: high (1,000/ liter), medium (500/liter), and low (OAiter). Three
164
replicates of each prey density were randomly assigned to the aquaria. Prey were introduced and tanks adjusted, with the use of a zooplankton counter, to the above densities three times daily (0830, 1130, and 1500 hours). Control tanks (0 Artemialliter) were given an equivalent amount of saltwater without brine shrimp at each feeding. The experiment was terminated after 8 days. Larval survival exceeded 60% in all but low-density treatments by the end of the experiment (Johnson & Dropkin 1995). Larval condition was significantly higher in medium- and high-density than in lowdensity treatments. We quantified larval behavior with a lap-top event-recording system (BEAST, Windward Technology, lnc., Kaneohe, Hawaii), having a latency of 55 ms for all keys. Eleven modal action patterns (MAPS; Barlow 1977) or types of swimming activity (Table 1) were recorded using focal-animal techniques (Altmann 1974) with 5-min observation sessions. A larva near the center of an aquarium was initially chosen and followed until no longer visible; observation then switched to a new individual near the aquarium center. These methods were used previously to characterize larval behavior (Ross & Backman 1992). Patch foraging theory was examined in relation to the timing of food introduction. Sudden prey introduction was used to simulate patch location by larvae. We recorded larval behavior in each tank 1 h before and 1 h after prey introduction. Larval behavior was quantified in this manner for one (midday) of the three prey-introduction periods per day for the duration of the experiment. In the second (prey deprivation) experiment, we placed 16-day-old larvae of the same origin into the nine 20-liter aquaria at a density of IOAiter. Protocols for acclimation, water temperature and exchange, and aeration were the same as those above. Artemia nauplii were added to three randomly assigned aquaria three times daily at a density of 1,000 naupliuliter to begin the first day of the experiment. Feeding at the same ration level was delayed until day three (2 days of food deprivation) for three additional groups and day five (4 days of deprivation) for the final three randomly assigned groups of larvae. Equal volumes of saltwater were again added to all aquaria regardless of treatment ration level; the study was terminated after 8 days. Mean 50% survival rates ranged from 3 to 5 days depending on treatment group (Johnson & Dropkin 1995). Both growth and condition were inversely related to the length of deprivation. Behavioral observations were made on days 1, 3, and 5 of the experiment both 1 h before and 1 h after prey introduction. Differences in “before” and “after” behavioral pro-
Foraging behavior of larval American shad files were interpreted as reversible behavioral effects of starvation. After several days of food deprivation, diminished responses to prey reintroduction that did not recover were interpreted as irreversible behavioral losses. To assess treatment effects on the orientation of larvae in the water column, we photographed the larvae in each aquarium the last day of the prey-density experiment and the sixth day of the prey-deprivation experiment. On photographic prints, straight lines were drawn through the longitudinal axis of each larva and the angle of each line from horizontal (possible range, 0 to 90") was measured. Parallax or related errors associated with this measurement technique were distributed equally among treatments because of the experimental design (randomly assigned tanks with replication). We subjected behavioral data from the prey-density experiment to two-way analysis of variance (ANOVA; SAS Institute 1987) for the treatment effects of prey density and introduction of prey (before or after). For two types of swimming behavior (swim freely and swim surface in Table l),the total time (s) spent performing each activity was used as the dependent variable; for all other MAPs or activities, frequency (the total number of acts or occurrences) was used. Data from the prey-deprivation experiment were subjected to one-way ANOVA for the effect of length of prey deprivation period. For those behavioral variables involving interaction with another fish (proximity, contact, and escape), the number of occurrences of each was indexed (total actdtotal larvae in aquarium) by the number of larvae in each aquarium to account for density variation. Observations of fish from the same tank were summed or averaged over successive days of the ex-
periment and not treated as independent observations (a violation of the assumption of independence of observations in ANOVA). Independent observations for inferential statistics were provided by observations of fish from different tanks. Repeated measurements of fish from the same tank were not used to build sample size in these experiments, as discussed by Machlis, Dodd & Fentress (1985) and Martin & Bateson (1993). We first converted larval orientation data to percent vertical values (range 0 to 100% vice 0 to 90"), then arc-sine transformed them. These data were subjected to one-way ANOVA for the treatment effects of prey density and deprivation period. Tukey's studentized range tests were used to examine differences in treatment means. Results
We observed significant prey-density effects for the activities pivot, dart, escape, sigmoid, and lunge (Table 2). Group means for the low ( O L ) prey density were lowest (direct relation, Table 2). Significant prey-introduction effects were observed for pivot, sigmoid, and lunge (Table 2). In each case the group mean was higher 1 h after prey introduction than that 1 h before food introduction (Table 2). Length of deprivation period (0, 2, or 4 days) exerted significant effects on two activities, pivot, and fixate (Table 3), regardless of whether larvae had returned to feeding after prey deprivation. In addition, significant effects were observed before return to feeding for dart and capture (Table 3). Relations between mean frequency of behavior and length of deprivation period were inverse (Table 3). Larvae held without food (low prey density) for
Table 1. Swimming activities and modal action patterns (MAPs) of larval American shad. Behavioral category
Activity or MAP
Description or definition
Swimming activity
Swim freely Swim surface Pivot' Dart
Active axial motion producing net movement through water column Active movement at water-air interface Orient or swim in a different direction by turning sharply (>45O) Swim at high velocity in straight line for more than two body lengths
lnteractivity
Proximity Contact Escape or avoid
Be in or move to a position within one body length of another fish Make contact or apparent contact with another fish, actively or passively Respond to onrushing fish by swimming away rapidly
Foraging
Fixate
~~
~~
~~
Position directly in front of suspended particle or prey without movementfor 21 s
SigmoidS Lunge Captures t
Body assumes a sigmoid or anguilliform curve Make short distance, high-speed burst toward suspended particle or prey item Remove food particle from water by ingestion
Similar to 'orientation" of Brown & Colgan (1984, 1985) except that orientation to a prey item was not always observed. Considered a feeding response by Brown & Colgan (1984, 1985). Subelement of ''lunge''in Brown & Colgan (1984, 1985); however, sigmoid was not always followed by rapid forward movement and thus is analyzed separately from lunge here.
165
Ross et al. Table 2. Results of analysis of variance for the effects of prey density (low, medium, and high) and time relative to prey introduction into aquarium (before and after feeding) on larval American shad behavior. Only statistically significant relations are listed. Means (fstandard deviation, SD) are the mean number of occurrences per 5 minutes. ~
Prey density Means (tSD)
Activity or
Medium
High
Fl 12
1.3k00.2 0.2f0.2
6.6k0.5 1.4H.2
5.7k1.O 1.0f0.5
18.62
0.01 *
13.59
0.006* *
1.8k0.3
3.3*0.7
4.7+0.9
8.07
0.02* 0.01
l.0f0.8 1.4k0.2
2.W0.5 2.410.5
1.9f0.4 1.510.0
14.10 7.47
P
F2.6
Swimming activity Pivot Dart lnteractivity Escape or avoid Foraging Sigmoid Lunge
Means (+_SO)
Low
MAP
52.71 9.32
9.21
0.0002*
~~~~
Food introduction effect
Before
After
0.001"
3.5k2.3
5.6k3.0
0.003" 0.02*
1.2fl.1 l.lkl.l
2.7fl.8 2.3i1.1
P
*, * * , * * * significantat 0.05.0.01, and 0,001
Table 3. Results of analysis of variance for the effects of length of deprivation period (days) on larval American shad behavior. Only statistically significant relations are listed. Means (+ standard deviation, SD) are the number of occurrences per 5 minutes for each deprivation period (0, 2. and 4 days). Before return to feeding
After return to feeding
Means (fSD) Activity or MAP
F2.6
Swimming activity Pivot Dart Foraging Fixate Capture
P
Means (fSD)
0
2
4
4,12
P
0
2
4
3.3k4.9
6.99
0.03'
11.7k3.2
6.8t1.6
10.8i1.8
7.10
0.03'
23.3k6.8
9.5k1.0
11.3i2.8
11.42 8.17
0.009" 0.02'
14.7k1.5 2.7k1.2
6.0k1.0 0.3f0.6
0.3f0.6
19.00 25.00
0.002*'
19.0k5.6 1.7t0.6
3.3k3.2 0
2.Ok1.0 0
0.001**
*, * *, significant at 0.05 and 0.01
the 8-day experimental period assumed an average angle (40°, head up) from horizontal twice that of the medium (21") and high (22") prey-density groups, which did not differ significantly from each other (Table 4). These larvae invariably oriented head-up. In the prey-deprivation experiment the same effect was observed after 4 days of deprivation (Table 4). Table 4. Results of analysis of variance and Tukey's studentized range test for treatment effects on larval orientation in water column in prey-density experiment (three levels of prey density) and deprivation-period experiment (number of days deprived).
Experiment
Prey density or deprivation period
Mean (+ standard deviation) angle from horizontal (")
F2,6
P
Prey density
Low density Medium density High density
40.4k2.1a 21.6fl .8b 22.1f4.3b
27.4
0.001*'
Deprivation period
Deprived 0 days Deprived 2 days Deprived 4 days
30.3f2.4b 29.1+4.8b 44.4k5.2'
14.1
0.005**
a,b
Tukey group (means with same superscript are not significantly different).
* * Significant at 0.01,
166
Discussion Our data support earlier findings (Lawrence 1972; Blaxter & Ehrlich 1974) that starving larvae exhibit reduced general activity levels. This reduction was observed in a number of discrete behavioral variables including the frequency of occurrence of pivot, dart, escape (avoid), fixate, sigmoid, and lunge. Pivot and dart represent behaviors that may increase the efficiency of either foraging or escape from predators (e.g., Johnson & Dropkin 1992). Escape or avoid may function to maintain inter-individual space for effective prey capture. Fixate, sigmoid, and lunge are stereotyped feeding responses found broadly among larval fishes (Blaxter & Hunter 1982; Brown & Colgan 1985). Our experiments were not designed to determine vertical-migration activity as were those of Blaxter & Ehrlich (1974). Variation in prey density affected elements of swimming activity (pivot and dart), interaction with other larvae (escape or avoid), and stereotyped feeding behavior (sigmoid and lunge). When larvae "found" food patches (simulated by sudden intro-
Foraging behavior of larval American shad duction of prey items into aquarium), one swimming activity (pivot) and two stereotyped feeding responses (sigmoid and lunge) increased in frequency. Brown & Colgan (1984, 1985) consider our pivot (their “orientation”) to be the initial feeding response of a series leading to prey capture. However, we could not determine this activity to be related to a prey item in every case. Interactions with other larvae did not change as a result of “arriving at a food patch.” As a whole, exposure to suboptimal prey densities for several days had a more profound effect on larval behavior (more MAPs affected) than did a sudden change in prey density, as simulated in this experiment. The foraging patterns,>? of larval American shad were consistent with the ciruise (active) search strategy, rather than ambush dr saltatory search, such as that employed by golden shiner larvae Notemigonus clysoleucas Mitchill (Browman & O’Brien 1992). To the extent that the fixed prey densities of our experiment represent submarginal, marginal, or supermarginal levels of energy present in discrete patches of food, the changes in behavior shown by larval shad support the patch model as a foraging strategy (Charnov 1976; Stevens & Krebs 1986). Elevated levels of pivot, dart, avoid, sigmoid, and lunge with increased prey density reflect “decisions” and mechanisms to stay in high-energy patches and continue to feed there. In similar experiments, the growth and survival of gizzard shad (Dorosoma cepedianum Lesueur) larvae were positively correlated with zooplankton prey density (Welker et al. 1994). The length of the prey-deprivation period affected larval behavior in somewhat different ways. Pivot (swimming MAP) decreased in frequency at longer deprivation periods both before and after return to feeding, while dart differed only before the return. Among feeding MAPs, fixate was reduced in chronically deprived larvae regardless of prey reintroduction, while capture was affected only prior to food reintroduction. Thus, the loss of pivot and fixate appears to represent an irreversible, pathological effect of starvation, with dart and capture being reversible. The irreversibly lost MAPs appear to function in the location of and proper orientation to prey items. Together, two of three categories of larval behavior (swimming and feeding, but not associative activities) were affected by the length of prey-deprivation period. Because these changes in behavior were accompanied by reduced growth and larval condition (Johnson & Dropkin 1995), we suggest they represent suboptimal levels of response normally needed for early riverine survival. Both prey density and deprivation period affected the orientation of American shad larvae in the water
column almost identically. The somewhat vertical, head-up orientation (42-44”) in deprived larvae probably ‘interferes with ability to swim to new food patches, as well as ability to execute adaptive feeding responses when prey are located. The latter conclusion was also inferred by Blaxter & Ehrlich (1974) in herring larvae; however, herring larvae displayed the opposite orientation (head-down) as a result of starvation. Blaxter & Ehrlich (1974) attributed this effect to catabolism of lipids concentrated in the head of larvae during starvation. The most likely explanation for the head-up orientation of our prey-deprived American shad larvae is lost ability to regulate the filling of otic bullae with gas. This process normally occurs at a larval size of 22-30 mm in herring but is species-specific (Blaxter & Hunter 1982). Thus, both prey density and length of prey-deprivation period affect larval behavior patterns related to swimming activity, association with other larvae, and stereotypical feeding responses. These changes in behavior may reduce the efficiency of location of food patches, pursuit and capture of prey items, or escape from predators. Some losses of behavior are irreversible, others reversible after moderate deprivation periods. Food deprivation may also result in anatomical changes in equilibrium or orientation (head-up) that further diminish adaptive foraging or escape responses. Optimal larval behavioral responses related to swimming activity, association with other larvae, and prey capture appear to be important determinants of larval survival in their early life history. In riverine systems that fail to meet minimum levels of prey density (undetermined, but 4 0 0 preykter) or patch frequency (2 to 4 days), larval survival may be reduced. Acknowledgements We thank J. A. Brown (Memorial University of Newfoundland), J. W. Meade, D. V. Rottiers, and C. W. Steele (Edinboro University of Pennsylvania) for comments on the manuscript and L. J. Mengel for statistical advice. M. Hendricks of the PennsyIvania Fish Commission provided the larval shad for the study.
Resumen I . Realizamos experimentos de laboratorio para determinar 10s efectos de densidades de presas sub6ptimas y de la duraci6n de pen’odos de ayuno en el comportamiento de natacion y social de las larvas de alosa americana A h a sapidissirnu. Empleamos tratamientos de 1000, 500 y 0 nauplios de Artemia por litro durante 8 dias y periodos de ayuno de 0, 2, y 4 dias. Durante 10s experimentos registrarnos la duraci6n o frecuencia de 11 tipos de comportamiento mediante un registrador de sucesos. 2. La exposici6n a densidades de presas sub6ptimas afect6 a las tres categon’as de comportamiento de las larvas: nataci6n (giro y aceleracih), social (huida y esquiva) y respuestas estereotipi-
167
Ross et al. cas de alimentacion (postura sigmoide y ataque). La localizacion de un parche rico en alimento, simulada mediante la introducci6n repentina de presas en el acuario, afecto a las frecuencias de las respuestas alimentarias m6s que a las otras categorias de comportamiento. El "modelo de parche" recibio apoyo como estrategia de alimentacion de las larvas. 3. Los efectos del ayuno se manifestaron sobre todo en cambios en el cornportamiento natatorio (menores frecuencias de giro y aceleracion subita), aunque las respuestas alimentarias (en especial fijacion) se redujeron tambien. La perdida de 10s comportamientos de giro y fijacion se revel6 como un efecto patol6gico e irreversible del ayuno. El ayuno produjo asimismo una mayor orientaci6n vertical de las larvas (cabeza hacia la superficie en Bngulo de 42" en larvas sometidas a ayuno, 21-29" en larvas alimentadas). 4. Estas alteraciones del comportamiento pueden conllevar una huida de 10s depredadores, localizacidn de parches de alimento o persecucidn y captura de presas menos efectiva en hibitats fluviales.
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