The effect of temperature and body size on digestive efficiency in Fundulus heteroclitus (L.)

The effect of temperature and body size on digestive efficiency in Fundulus heteroclitus (L.)

J. up. 0 mar. Biol. Ecol., Elsevier/North-Holland 1979. Vol. 38, pp. 179-186 Biomedical Press THE EFFECT OF TEMPERATURE AND BODY SIZE ON DIGES...

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J. up.

0

mar. Biol.

Ecol.,

Elsevier/North-Holland

1979. Vol. 38, pp. 179-186

Biomedical

Press

THE EFFECT OF TEMPERATURE AND BODY SIZE ON DIGESTIVE EFFICIENCY IN FUNDULUS HETEROCLITUS

Department

T!MOTHY E. T.ARGETT qf Maine, Orono,

qfZoo:oology, University

Maine,

(L.)

U.S.A

Abstract: The digestive efficiency of temperature acclimated mummichogs, Fund&s heteroclitus (L.). was detet;mined using the amphipod Orchestia grillus BOX as prey. Experiments were conducted on three size [email protected] of mummichogs ( 3 g) at 5. 13, 21, and 29 “C. No difference was found in digestive efficiency by different sizes of mummichogs. There was, however, a statistically significant difference in efficiency over the range of acclimation temperatures, with the efficiencies being temperature independent from 13 to 29 “C and dropping slightly at 5 “C. From 13 to 29 “C. digestive efficiencies were the maximum possible. Temperatures in this range are normal late spring, summer, and early fall habitat temperatures in Maine estuaries. The ability to maintain a maximum efficiency of digestion over this 16°C temperature range allows mummichogs to get the maximum amount of energy from their prey during the time of year when they are utilizing substantial energy for growth (somatic and gonadal) and for activity (foraging and mating). The digestive efficiency at 5 “C was only about 13.5”” less than at 21 and 29 “C. This drop is probably of little ecological or energetic significance, so that mummichogs are actually able to absorb food energy across their alimentary tract relatively independent of acclimation temperature over a 24 “C range.

The mummichog, Fundulus heteroclitus (L.), is an abundant fish in shallow estuarine waters and salt marshes along the eastern United States. It is the most common fish in the tidal marshes of New England (Valiela et al., 1977). Several recent papers have dealt with food and feeding in this fish (Jeffries, 1972; Prinslow et al., 1974; Vince et al., 1976; Baker-Dittus, 1978; Kneib & Stiven, 1978), but little is known about the efficiency of digestive processes. Babkin & Bowie (1928) found that mummichogs have no true stomach (i.e. an organ secreting pepsin and hydrochloric acid) and that digestion takes place under alkaline conditions. Schmelz (1964) observed that much of the plant and animal food consumed appeared to pass out of the fish with little enzymatic alteration, and that it was not known how efficient the alkaline system was in digesting food. Prinslow et al. (1974), working with fish acclimated to 13 “C, found a maximum conversion efficiency (energy of new tissues/energy of food consumed) of 9% when the fish were fed a ration of 6% dry body weight/day, but no experiments were done on digestive efficiency. Mummichogs experience wide habitat temperature fluctuations seasonally (e.g., 635 “C in a Delaware salt marsh; Schmelz, 1964). The relationship of respiratory metabolism

to acclimation

temperature

shows that mummichogs 179

are well adapted

180

TIMOTHYETARGETT

metabolically to life in such environments (Targett, 1978). This species exhibits a zone of relative thermal independence of respiratory metabolic rate from 13-29 “C, thus conserving energy reserves over upper temperature ranges that would require rapid energy turnover if respiratory metabolism were more temperature dependent. Furthermore, a substantial reduction of metabolic processes between 5 and 13 “C conserves metabolic reserves during the coldest months, allowing fish to draw upon them for increased activity and metabolic rate when suitable environmental conditions return. The only study investigating the effect of temperature on digestion in mummichogs is that of -Nichoiis (1933) who showed that digestion rate, iipase activity, and intestinal motility increased with temperature. Experiments were conducted at temperatures from 5-29.5 “C, but the fish were acutely tested (given no time to acclimate to the experimental temperatures) after being held at 15-19 “C. It is not surprising, therefore, that no digestion was found below 6 “C or above 29.5 “C. No information is available on digestive efficiency in the mummichog or how it responds to temperature change. It is not known if an efficient level of digestion can be maintained over the wide temperature range experienced seasonally by this fish. Also, there are no data on the effect of body size on digestive efficiency. The purpose of the present study was to investigate the effects of temperature and body size on digestive efficiency in the mummichog.

Mummichogs were seined from shallow estuarine mud flat tide-pools at PenobScot, Maine in upper Penobscot Bay. In the laboratory, fish were placed into aquaria containing aerated artificial sea water (Instant Ocean, Aquarium Systems Inc., Eastlake, Ohio) at a salinity of 30 %,,,and acclimated to 5, 13, 2 1, and 29 “C. Acclimation time ranged from seven days to more than two months, with most fish being acclimated for at least one month. Amphipods. Orchestia grillus Bose, were chosen as the food item because amphipodsare important prey for mummichogs in nature (Schmelz, 1964; Nixon & Oviatt, 1973; Fritz, 1974; Vince et al., 1976; Kneib & Stiven, 1978). 0. grih of z 10 mg dry body weight were collected sup~dlittorally at Penobscot, Maine and were starved for 24 h before being fed to mummichogs. The starvation period functioned to clear the amphipods’ alimentary tracts of all plant material, an undigestible item for mummichogs. After the acclimation period, fish at each of the experimental temperatures were separated into three size groups ( < 1 g, l--3 g, >3 g). Approximately 15 < l-g fish, 10 i-3-g fish, and 5 >3-g fish were placed into three separate 6.5-l aquaria containing aerated artificial (30x, S) sea water and maintained at their acclimation temperature. Approximately 15 0. grilhs were placed into the aquarium containing cl-g fish and ~20 were placed into each of the aquaria containing l-3-g and >3-g fish. Fish

DIGESTIVE

EFFICIENCY

IN FUNDULC’S

181

fed voluntarily and fecal material was collected by siphon from the aquaria bottoms. The first collection of feces was discarded to prevent contamination of fecal material by any food present in the fishes’ alimentary tracts when the amphipods were eaten. Following this, the fish were fed as before and the feces collected (no longer than 12 h after being produced).

Fecal material

was microscopically

examined

and scales

and small pieces of mucus sloughed from the lining of the gut were discarded. Excess water was removed by pipette. Fecal material and a sample of five live amphipods were dried at 60 “C. This feeding, feces collecting, and drying procedure continued untii there was enough materiai for caioric anaiysis. The four dried sampies from each experimental temperature (one food sample and a fecal sample from each size group) were stored at - 10 “C until caloric analysis. Upon analysis. each sample was homogenized in a Wig L Bug homogenizer and calories/mg dry wt determined using a Phillipson microbomb calorimeter (Phillipson. 1964) and standard procedures (Crisp, 1971; Paine, 1971; Schroeder, 1977). Two caloric content determinations were done on each sample. A ~3% difference between the two values was considered acceptable accuracy (Golley, 1961; Paine, 1971). In three cases the two caloric values differed by more than 37, and a third was determined. This value was invariably within 3”/, of one of the originals and the other was discarded. In two other cases (5 ‘C, < i-g fjsh and 29 “C, < i-g fish) insufficient fecal material prevented a third calorie determination and it was necessary to accept a >32, difference between values. Percentage ash was determined for each sample by igniting at 500 “C for 4 h. Digestive efficiencies were determined by an ash indicator method (Conover, 1966). Calculations, using symbols from Warren&Davis (1967), were done according to the following

equation

: Digestive

efficiency

= 9, c

where Q, is energy content of the food in cal/mg ash wt and Ql, is energy content of the feces in cal/mg ash wt. Mean digestive efficiency was calculated from the duplicate values for each size group at each experimental temperature.

RESULTS

Digestive efficiencies were constant for different sizes of mummichogs and intemcreased slightly from ‘the low 70% to the middle 80 7; range with increasing perature (Table I). Two-way analysis of variance showed no significant difference (F = 0.288 ; d.f. = 2, 6; P > 0.75) in digestive efficiency by different sizes of mummichogs. A significant difference (F = 17.325; d.f. = 3, 6; P < 0.01) was found, however, in digestive efficiency over the range of acclimation temperatures. Comparison of mean digestive efficiencies for the four temperatures by Tukey’s w-procedure

TIMOTHY

182

E. TARGETT

(Sokal & Rohlf, 1969) showed that the values fell into two groups. The 5 and 13 “C digestive efficiencies were not significantly different and those at 13, 21, and 29 “C were not significantly different. Thus, mummichog digestive efficiency is temperature independent from 13 to 29 “C and drops slightly at 5 “C. The drop in

Digestive efficiencies in three size classes of Fun~c~~~/.~ ~ii~~er~~lji~.~at the four acclimation means not underscored by the same line are significantly different (Tukey’s x-procedure; Acclimation

(“C) -_-.

Body weight (g)

5

13 -

21 .-


73.9 70.0 75.3

82.2 81.8 75.2

86.2 57.5 87.8

87.2 86.0 85.7

73.1

79.1 I________-

87.2

86.3

Mean

&j&q~

temperature _

temperatures: P < 0.01).

at _S“C is only

4ipht hnwever _^_D_‘_, __- . _.

__, wit!h. the _S“C &ppc;tivP m--‘- - pffi&nq

29 -. ._.- -

being

jpss

than that at 21 and 29 “C by only about 13,.5:/o.This is probably of little ecological or energetic significance. Absorption of food energy across the alimentary tract of mummichogs is, therefore, relatively independent of acclimation temperature over a 24 “C range. DISCUSSION

Although mummichogs have no true stomach and digest food under alkaline conditions, digestive efficiency is similar to that in other fishes feeding on organisms having chitinous exoskeletons. Elliott (19’76) found digestive efficiencies to range between 78 and 85% in Salmo trutta fed the amphipod Gammarus pulex at a ration of one half maximum. Pandian (1967) reported that Megulops cyprinoides and Ophiocephalus striatus feeding on the prawn Metapenaeus monoceros digested and absorbed about 90% of the energy, exclusive of undigestible chitin. Because the chitin content of the prawn was 5% ofdry body weight, the overall digestive efficiency would also be in the middle 80% range. Mummichog digestive efficiency is independent of body size. This agrees with the results of several workers on other fishes. Digestive efficiency of total food energy was found to be independent of body size in Ep~nephelus gut&&s (Menzel, 1960), ~e~~~~ps cypr~n~~des(Pandian, 19671, Oph~5cepha~usstrifftus (Pandian, 1967; Vivekanandan, 1977), Fundulus notatus (Atmar & Stewart, 1972), Blennius pholis (Wallace, 1973), Salmo trutta (Elliott, 1976), and Ophiocephalus punctatus (Gerald, 1976a, b). The protein fraction of the diet, when analysed separately, was also found

DIGESTIVE

EFFICIENCY

IN FUNDULUS

183

to be absorbed independently of fish size in Le~o~is cya~el~us and L. ~eg~i~~~s (Gerking. 1952), Epi~ep~eIus gutfatus (Menzel, 1960), and Megalops ~ypr~~~oidesand Ophiocepphalus striatus (Pandian, 1967). The same pattern was found for the lipid fraction of the food in Epinepheius guttatus (Menzel, 1960). A constancy of digestive efficiency with changing body size within fish species seems, therefore, to be a general rule. The relative constancy of mummichog digestive efficiency over a 24 “C range of acclimation temperatures may represent an adaptation to the thermally variable habitat in which mummichogs live. Assuming that most of the energy expended in foraging for food and absorbing energy from it is involved in foraging, then it is energetically advantageous for mummichogs to absorb a maximum amount of energy from their prey at ail normal habitat temperatures. This is essentially the case. The digestive efficiencies at 13, 21, and 29 “C are the maximum efficiencies possible on amphipod prey. At these three temperatures, the fecal material consisted almost entirely of undigestible chitin. There was a small fraction of other undigested m.aterial at 13 “C. but the f&h were still nmrlv a!! the av&&!e pnprgy -_-- _ ahwrhinp _“_______D -‘_-‘~, from the amphipod prey. At 5 “C there was more non-chitin material (available energy not absorbed) in the feces, but the drop in efficiency was oniy by 6.6”, from that at 13°C. The ability of mummichogs to maintain an efficient level of energy absorption over a wide temperature range could be due to several factors. It was observed that the rate of digestion was slower as temperatures decreased, with the first fecal material appearing ~4 h after feeding at 29 “C, ~7 h at 21 “C, z 15 h at 13 “C. and ~24 h at 5 “C. Longer residence time at lower temperatures could allow the enzymatic reactions of digestion and absorption, which may be slowed as temperatures C~P~TPR~P eygnti&~ CROP nrnnnrtinn ac UC St hiohmtwnner~J the c..v “uIIIw y’“y”’ LlVl. nf VI PTIPI‘OV W”“‘bJ UY “‘b”.,’ c”““yuAu _--- “_“.-, tn ,- extract tures. The relative constancy of digestive efficiency could also be due to temperature comI~ensation of enzyme function. Smit (1967) showed that the gastric secretion rate of Ictalurus nehulosus was 687” greater in 20 “C acclimated than in 30 “C acclimated fish, when tested at 25 “C. Owen & Wiggs (1971) found that extracts of Sulvelinus fbntinalis gastric mucosa had 307; greater activity in 5 “C acclimated than in 12 “C acclimated fish. They attributed this to a greater quantity of pepsinogen in the cold acclimated trout. Relative thermal constancy of digestive processes in mumxnichogs is at least partially due to acclimation or temperature compensation phenomena because Nicholls (1933) found no digestion below 6 “C or above 29.5 “C in acutelytpctpC1 LIULV.. mllmmirhnoc “‘Y.“““““‘.V~“. Other studies have shown digestive efficiency to be temperature independent. Menzel (1960) found digestive efficiencies in Epinep~le~Lt~~ gutratus to vary between 91.3 and 97.37; over the temperature range from 19 to 28 “C. Wallace (1973) found digestive efficiencies to be 95-97 y0 in Blennius pholis acclimated to 10 and 25 “C. Gerald (1976b) showed that the efficiency of digestion was between 93 and SS;, in Ophiocephalus punctatus acclimates to 20, 28, and 33 “C. Finally,

184

TIMOTHY

E.TARGETT

Vivekanandan & Pandian (1977) found that digestive efficiency in 0. striates was between 94 and 98”//,over the temperature range from 17 to 37 “C. Two other studies have found digestive efficiency to be temperature dependent over at least part of the temperature range, but to change by only a few per cent. Digestive efficiency in Salmo gairdneri was found to be 72‘;G at 5 “C, 78:/d at 17 “C, and S50/ at 20°C (Brocksen & Bugge, 1974). These findings, however, may be a result of the fish acclimating to the experimental temperatures for only 48 h prior to the experiments. Digestive efficiency in S. trutta depended upon the size of the ration, but increased from x7&80”/;, at 4 “C to %80-9O”i, at 20°C (Elliott, 1976). All of the above studies have shown a relative constancy of digestive efficiency generally over a range < 15 “C. The only other study showing a constancy of energy absorption efficiency over a temperature range approaching that found in the present work is the constancy over a 20 “C range reported by Vivekanandan & Pandian (1977). Their experimental fish, Ophiocephalus striatus, lives in shallow freshwater habitats in the tropics and also experiences considerable seasonal habitat temperature changes (Jhingran, 1975). Temperatures between 13 and 29 “C are normal late spring, summer, and early fall habitat temperatures in Maine estuaries. Maintenance of a maximum digestive efficiency from 13 to 29 “C permits mummichogs to obtain the maximum amount of energy from their food during the time of year when they are utilizing substantial amounts of energy for growth (somatic and gonadal) and for activity (foraging and mating). This ability complements the pattern of conserving energy for these purposes indicated by relative thermal independence of routine respiratory metabolism from I3 to 29 “C (Target& 1978). Furthermore, because the digestive rate increases with temperature, the daily ration or amount of energy absorbed per unit time also increases, thus yielding more energy for metabolic processes and growth over the upper temperature ranges. The slight drop in digestive efficiency at 5 “C coincides with a large drop in routine respiratory metabolic rate at that temperature (Target& 1978). Mummichogs are, therefore, able to absorb a maximum amount of energy from their prey after acclimation to normal late spring, summer, or early fall habitat temperatures, and are also able to maintain a nearly maximum efficiency at temperatures experienced during the coldest months.

ACKNOWLEDGEMENTS

I thank Drs J. H. Dearborn, R. B. Owen, and J. M. Shick for use of their laboratory space and equipment, Mr D. M. Wyanski for help collecting fish and amphipods, and Dr E. F. Lowe for many helpful conversations regarding the research. Thanks also go to Drs R. B. Owen, J. G. Stanley, B. D. Sidell, J. H. Dearborn, and MS N. M. Targett for their helpful comments on the manuscript.

REFERENCES

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AI

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