Distribution, Growth, and Seasonal Abundance of ...

Distribution, Growth, and Seasonal Abundance of Hyulella azteca (Arnphipoda) in Relation to Sedirnent Microfloral J. Fish. Res. Bd. Can. Downloaded from www.nrcresearchpress.com by Harbin Industrial University on 06/06/13 For personal use only.

Bannv T. HencnavB2 DePartment of ZooIogY [Jn'ivers'ity oJ Bri't'ish Columbia, Vancouaer 8, B'C. 1970. Distribution, growth, and seasonal abundance of Hyalella H.q.ncnevp, B. T. azteca (Amphipoda) in relation to sediment microflora. J. Fish. Res. Bd. Canada 27: 685-699. Growth, density, and body size of the deposit-feeding amphipod Hyalell'a azteca, and its food, epibenthic algae, and sediment microflora, were greatest in shallow-water areas of Marion Lake. The vertical distribution of Hyalella was limited to the upper 2 cm of sediment cores. Highest concentrations of sedimentary chlorophyll and lowest concentrations of nondigestible ligninlike material also occurred at the sedin'rent surface. In laboratory substrate-choice experiments, Hyalella differelrtiated between sediments with different concentrations of microorganisms, and growth depended upon the quantity of microflora in the diet. In Marion Lake, increased growth of Hyalello during June was independent of temperature and closely correlated with iucreased rates of epibenthic primary production. Egg production, related to body size in a uonlinear manner' began during May as growth rates increased. As a combined result of egg production and juvenile survival, the maximum density of Hyaletla in Marion Lake was reached in August' Received

April

24, 1969 INTRODUCTION

CoupenrsoN oF ECoLocrcAL coNDITIoNSwithin areas of high and lorv density of animal species may suggest factors that influence their distribution. The present study considers the distribution of a freshu,ater benthic amphipod, Hyal.el,loazteca (Saussure), from such a point of view' Previous studies in Marion Lake have shown that Hyalella is most abundant in shallow-water sediment (less than 2 m) and almost absent from the deeper parts of the lake (5 m) (Hamilton, N4S, 1965; Mathias, MS, 1967). This depth distribution corresponds directly to the attenuation of light and decreasein epibenthic algal production *ith depth in N{arion Lake (Hargrave, 1969). Laboratory experiments have also indicated that Hyalella digests bacteria and algae from ingested sediment particles (Hargrave, 1970)' Thus, iI this food source is important in determining amphipod distribution, some relation between epibenthic primary production and numbers of. Hyalella would be expected. This study compares the horizontal and vertical distribution, daily growth rate, and seasonal abundance ol Hyalello with sediment microflora production and indices of digestible sediment organic matter. lCanadian Contribution to the International Biological Programme No. CCIBP-52. 2Present address: Freshwater Laboratory, Hillerld, Denmark.

685 Printed in

Canada

(J1458)

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JOURNAI, FISHERIES RESEARCH

J. Fish. Res. Bd. Can. Downloaded from www.nrcresearchpress.com by Harbin Industrial University on 06/06/13 For personal use only.

MATERIALS

BOARD OF CANADA.

AND

VOI,.2i.

NO. 4. 1970

METHODS

All rnaterials were takeu from sediments in Marion Lake, 8.C., previously described by EITord (1967). Undisturbed dredge samples were taken at least once per rnolth during 1968 by methods described by Hargrave (1969). The soft ooze sediments (gyttja) from various depths of the lake were either sieved (rnean mesh size 0.25 rnm) or sampled by glass cylinders (12 X 5 cm) (Hargrave, 1969). This allowed both total numbers per unit area and the vertical distribution of Hyalella within sediment cores from different areas to be compared with different measures of sediment organic matter. Hylella was separated from sediment sections by sieving, so that amphipods became trapped in the surface film of water over the sediment. Movement of animals trapped in the surface film allowed even the smallest instar stages to be collected. The densities of amphipods enumerated in this manner compared well with samples taken by the sugar flotation technique (Anderson, 1959) as used by Mathias (MS, 1967). Amphipods were enumerated, eggs were counted when present, and all animals were dried at 50 C for 12 hr before weight determinations were made with a Cahn electrobalance (+1 pg) in an external weighing chamber held at 50 C. This drying temperature prevented loss of volatile organic substances, as recommended by Lovegrove (1966). Sectioning of sediment cores was done immediately after the core was taken by pushing the lower end of the core with a plunger and slicing consecutive l-cm sections from the top with a sharp edge. When amphipods had been separated from each section, sedimentary chlorophyll and acid-insoluble matter were determined (Hargrave, 1969, 1970). The importance of microflora on sediment as food for Hyalella was examined by measuring the changes in dissolved oxygen concentration over undisturbed sediment cores, which provides an index of benthic algal production. The technique is described by Hargrave (1969), The vertical distribution of oxygen and, pH in undisturbed sediment cores was measured by .inserting a Beckman oxygen probe and pH electrode into the sediment immediately after sampling. Care was taken not to disturb stratification within sediment cores. Substrate-choice experiments were used to determine the effect of sediment microflora on Hyalella distribution. Substrate-choice experiments have been used to demonstrate the ability of benthic invertebrates to select substrates of a certairr grain size (Wieser, 1956) or particles with certain microorganisms on their surfaces (Wilson, 1955; Meadows, 196i1; Marzolf, 1965; Gray,1967). During each of the four substrate-choice experiments, Hyalella was offered surface sediment treated to alter the microflora content. Diatoms (Noaicula sp.) were cultured from Marion Lake sediment. A slurry of cells and sediment was filtered by vacuum to increase cell numbers in the sediment. Streptomycin-(SOa) and neomycin (50 mg/liter) were used to inhibit bacterial growth. Other sediment sarnples were autoclaved and rinsed with lake water. Untreated surface sediment served as the control. Sediment preparations were placed in a 50 X 15 X 10-cm plexiglass trough in sufficient quantity to cover the bottom to a depth of 2 cm. Each sediment type was adjacent to the other so as to form a continuous cover over the bottom. Lake water (1 liter) was slowly added from one end so that the sediment rvas undisturbed and 35 llyalella were evenly distributed into water over the sediment. The trough was left for 24 hr in the dark before amphipods in each sediment type were enumerated. To examine the importance of algae in determining the growth of Hyal'ella, Chara with attached epiphytes was collected from around springs in Marion Lake. This food source was rich in living microflora and assimilated with over 65le efficiency, in contrast to surface sediment, whlch Hyalello digested with 10-15/, efliciency (Hargrave, 1970). Amphipods were collected, divided, and weighed immediately to give an initial estimate of the weight-frequency distribution and establish the reproducibility in subdividing the population. The remaining two groups of amphipods were placed in culture dishes rvith 200 ml of lake water. One group was offered Chara with epiphytes (10 g wet weight); the other was provided with samples of surface sediment (5-10 g wet weight). The cultures were held at 8 C on a 72-hr light-dark cycle and renewed every 4 days, when fresh Chara and sediment were added. After 30 days amphipods from both

687

HARGRAVE: HYALELLA AZTECA AND SEDIMENT MICROFLORA

culture dishes were removed, dried, and weighed. Growth rates were calculated by comparing amphipod mean dry weight at the beginning and end of the 30-day period. I{ESUI,TS


DISrnreurroN The restricted depth distribution of Hyalella (Hamilton, N'{S, 196.5; Nlathias, NIS, 1967) has been apparent during the present study (Fig' 1)' The marked decreasein density belotv 2 3 m u'as found in all samples taken during 1968. There was also a cofresponding decreasein amphipod body size (dry weight) with increasing depth of \'vater over the sediment (Fig. 1)'

E

350 6;

600

o

'l 5UU ol

enn

c o o

3

Nl II

250 E ol -ol

o, o E

^^^ x

.vw

-l

z Frc. 1. Density and. dry.weight. of -adult Hyalella dzl?co at varlous depths ln ivlarlon Like durins Mav 1968. Densiiy ol Crangonyx richmondeniis occidentalis also illustrated. All ooints are means of at least three determinations. Vertical lines represent standard errors of the mean.

1.0

3.0 2.O Depth (m)

4.O

The decrease in number and lveight ol Hyalel,la with increasing depth suggestsa direct relation between amphipod dry lveigl-rtand density. Intensive ."*pti"g at various depths during May 1968 showed such a relation to exist for densities up to 20 amphipods per Eckman sample; however, at higher densities dry weigl-rt and density appeared to be inversely related (Fig. 2). Examination of antennal segment numbef (2I-25) and head length (0.550.66 mm), as described by Cooper (1965), showed that only adult Hyalella were present in the population. Thus, differences in mean body weight at various depths do not reflect a shift in age structure but indicate adults of a smaller size with increasing deptl-r of water. PHYSICAL

FACTORS

The differences in size and density of. Hyatetla observed with depth in \llarion Lake could be due to many factors. Physical conditions seem to be of little importance. pH is relatively constant and ranges from 6.6 to 6.9

688


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JOURNAL

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RESEARCH

BOARD OF CANADA,

VOL.27,

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ouu

.3 400

=

i goo l9 -ol d i

Relationship between density and dry weight Frc. 2. of adult Ifyalella ozteca in Marion Lake during May 1968. Points are individual samDles, vertical lines indicate standard error of mean amphipod dry weight per sample.

200

in surface sediment from various depths; in 1968 the well-mixed water column supplied oxygen to all depths at near saturation levels, and temperature differences seldom exceeded 5 C (Hargrave, t969). The sediments in N{arion Lake are a gyttja, which contain 351570 organic matter (loss in weight after t hr at 600 C) and consist of aggregates of colloidal particles. There was a significant difference in total organic matter in surface sediment (top 1 cm) only in sediment covered with more than 4 m of water: Depth (zz) Organic matter (o/p) :L SE

0-1 3 7. 8 0.3

r-2 3 7. 9 0.2

2-3 s7.7 0.3

34 37.7 0.3

4-5 38.4 0.4

5-O 4I

. J

1.2

Both the color and texture of sediment varied with depth. Sediment collected in deep water contained fragments of leaves and bark and was dark brown in color and of fine silty consistency, whereas shallor,v-watersediment was a light brown color and much more clumped. The texture of shalloi,v-water sediments was largely due to the distinct algal-mat layer and numerous chironomid tubes, which served to form a spongy semisolid mud-water interface. The algal-mat layer and netr'vork of chironomid tubes was much reduced in sediments below 3 m. Numerous r't'orkers have stressed the importance of cover in influencing spatial differencesin numbers of benthic organisms. In Marion Lake, Hyalella occurs largely on open sediment and does not shorv any contagious distribution associated with beds of. Potamogetonor Chara. The density and mean dry weight of amphipods taken from these areas were not significantly different from samples taken on adjacent open sediment:

HARGRAVEI

HYALELLA

AZTECA

AND

Chara


Hyalella dry weight (pg :t sa) No./m2

289+32 310

SEDIMENT

689

MICROFLORA

Potamogeton

310+21 345

Sediment 290t19 ,'t.tJ

The decrease in numbers and size of Hyalella with increasing depth of water over the sediment parallels the attenuation of light with increasing depth. Laboratory and field observations have shourn that in N'Iarion Lake an average of 80/6 of the amphipod population is 1r'ithin the sediment (D. Ware, personal communication) and this proportion is affected by light and temperature. Observations during the present study confirmed the tendency for amphipods to align themselves against a surface or under objects such as pieces of leaf. PREDATION

AND

MIGRATION

If the factors of natality, mortality, and movement operate in a nonrandom way, changes in population size and structure may vary in different areas. In Marion Lake, trout (Salmo gaildneri Richardson), kokanee (Oncorhynchus nerha Walbaum), and salamanders (Ambystorna gracile Baird and Taricha granulosa Skilton) feed on Hyalella (Hamilton, tr"IS,1965). There is, however, at present no evidence to suggest that these predators are more nurnerous in deeper water. In addition, N'Iathias (NIS, 1967) showed that instantaneous mortality rates of adult Hyalella in shallorv and deep rvater were similar and egg and young mortality ranged from 70 to 80/6 in shallow and deep u'ater, respectively. Thus, if this mortality is primarily due to predation, the effects appear to be similar at all depths. \4ovement behavior of both species of amphipods in Nlarion Lake is currently being studied (A. Bryan, personal communication). Laboratory and field observations have suggestedthat amphipods move extensively over an area of a few meters distance, but there is little evidence of movement from shallorv to deep water. IMathias (I,IS, 1967) suggestedthat a sudden increase and decrease in numbers oI Hyalella in deeprvater sediments during August 1966 rvas due to immigration from shallow water follor'ved by emigration. These differences were not observed during the present study, but it is likely that the 3- to -lveek sample interval \vas too large to detect such shifts in population density, if they do occur. Changes in spatial distribution ol Hyatetta might occur by means of swimming activity. Hyatetta lvere never found in samples taken by towing a fine-mesh plankton net at various depths during the night and day on several occasionsduring 1967 and 1968. Also, zooplankton samples taken during t967 by a high speed suction pump (l'IcQueen, 1969) contained no Hyalell'a' If movement occurs on or close to sediment surfaces, horvever, these sampling methods r'r'ould not be adequate. FOOD

SUPPLY

In Nlarion Lake, Hyalello is predominantly a deposit feeder, which digests algal and bacterial cells from ingested surface sediment material (Hargrave, Ig70). Chara and epiphytes are also extensively bror,vsedand dead leaf material


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FISHERIES RESEARCH

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No. 4. 1970

is ingested. Hyalella is also reported, however, to feed on freshly killed animal flesh of various types, attack wounded isopods, and eat its own dead (Embody, I9l2). These observations could not be substantiated during the present study. Dead specimens of both Crangonyr and Hyaletla were offered as the only source of food to freshly collected Hyalella. No evidence of ingestion or egestion was found after 3 weeks. Possible correlation between Hyalella density and sediment organic material available for digestion was examined in trvo ways. During 1968, primary production by epibenthic algae on sediment at different depths in \tlarion Lake was measured (Hargrave, 1969) and compared u'ith total numbers of Hyalella: Depth (m) Epibenthic primary production (e C/me per year) Total mean density of Hyalella/m2 X 702

0-1 4 7. 9 37.5

l-2 41.5 12.O

2-3 31.0 4.0

34 28.r 0.9

4-5 2 7. 0 0.8

Amphipod density calculations are similar to those made by Hamilton (NIS, 1965) and Mathias (N'IS, 1967). Both Hyalello numbers and epibenthic algal production decreased in a nonlinear manner with increasing depth of water over the sediment. The decline in amphipod numbers, holever, was much greater than that observed in primary production. \lleasures of epibenthic primary production consider total algal productivity and do not indicate important species differences that occur at various depths. For example, in September 1968, diatoms were numerous on sediments covered with 1-2 m of rvater. Above and below this depth the standing crop of diatoms declined (G. Gruendling, personal communication). Similar differences have been found in spatial distribution of green and blue-green algae. In laboratory experiments (Hargrave, 1970), Hyalella digested different species of sediment microflora with different degrees of efficiency. Diatoms u'ere digested readily (707;, but the blue-green alga Anabaena sp. was not (15%).These differences in assimilation indicate that not all epibenthic algal production is available to Hyalella and illustrate the difficulty of comparing amphipod biomass rvith total epibenthic algal production. Sedimentary chlorophyll and ligninlike (acid-insoluble) material were measured in three replicate (2) sediment cores taken from depths at u'hich amphipod samples r'vere taken for comparison with amphipod distribution (Fig. 3). Although total organic matter in sediment above 4-m depth showed little variation with depth, both sedimentary chlorophyll and lignin content showed the largest gradients within the upper 2 cm. Hyalello showed a similar vertical distribution. In both substrate-cl.roiceexperirnents, sediment to rvl-richdiatoms u'ere a d d e d c o n t a i n e d t h e g r e a t e s t p e r c e n t a g eo I H y a l e l l a ( F i g . 4 ) . T h e r e \ r a s n o significant difference betr'veenthe numbers found in the sterilized sediments (D-n* : 24.5; P :0.245), as evaluatedbya I(olmogorov-Smirovonesample test for goodnessof fit (Siegel,1956). Amphipods in diatom-enriched and natural

HARGRAVE:

HYALELLA

AZTECA

AND

SEDIMENT

Lignin

N' H um ; ; ibt e Xrt o , oxvqen


as-pm-t

mg/l

691

MICROFLORA

I

as

of total organics

z organic matter

Sedimentary chlorophyll units/g

of Hyalella Frc. 3. Vertical distribution azteca, dissolv ed oxygen conce ntration, lignin' sedimentary and organic maiter, total chlorophvil in sediment cores from various deoths in Marion Lake. The average of d u b- l i c a t e s a m p l e s t a k e n d u r i n g J u l y 1 9 6 8 is illustrated.

-gt +q d 1-e

Frc. 4. Duplicate substrate-choice experiments to consider-the distribution of Ityalella asleca after 24 hr in sediments treated in various ways to alter microflora content.

ho 0.^

z d i a t o m s antibiotic natural su1961sys6 added s t e r i l i z e d s u b s t r a l e

Treatment

sediment also had darker gut contents than those in sterilized sediments, indicating reduced ingestion in the latter. The antennae, which bear many small club-shaped appendages, appear to be important in Hyalella's response to the sediment. The bristles on the antennal flagella have been shown to function as taste organs (Waterman, 1961) and this rvas appafent during feeding activity. The antennae continually move and touch the sediment when Hyalella is not feeding, but while it is browsing they are stationary on the sediment surface' GnowrH R,q.rs During its 12- to 16-month life span, Hyalelta grows from an egg (dry rveight 14 pd to a mature adult (dry weight 700-1000 pg) (Fig. 5). Differences in sizesof amphipods taken from different depths in Marion Lake were apparent throughout 1967 and 1963 (Fig.5). Growth rates of young and adult Hyalella, as derived from changes in body dry rveight during 1968, are presented in Fig. 6. Growth rates of juveniles are underestimated because of continued recruitment during the summer months. Egg production ceased during September, however, and gror,vth rates thefeafter are not affected by this error' Grou,th rates estimated from changes in biomass of the natural population will also be underestimated to the extent that larger a1-rphipodsare preferentially preyed upon (size-specificmortality). N4athias (N1ls, 1967) showed that instantaneous mortality rates of aduJt Hyatella in shallow and deep water (1965) are similar. Thus, if size-specilicmortality occurs, as found by Cooper all depths at equally act to it appears and D. ware (personal communication),

JOURNTAL I..ISHERIES RESEARC H B O . \ R D O F C . A N . \ D A , V O L . 2 7 , N O . 4 , 1 9 7 0


o _a

.st

;

Frc. 5. Growth curves for HyalelLa azteca at various depths in Marion Lake durine 1968. Points are means of three determinations. Vertical lines indicate standard error of mean.

dl

ol 6l rl

AODFAJA Time(months)

production H

Frc. 6. Conrparison of growth rate ol Hjalella azteca and eprbenthic primary production on sediment at 1.0-rn depth in Marion Lake during 1968. Juvenile and adult growth rates shown seoaratelv.

5 4mg E' 3OO a N