PART IV: ASSIMILAT ION EFF ICI ENCY, EGESTION, AND EXCRETION OF ZOOPLANKTON AND BENTHOS

I ntroduction

203 . Assimilat ion (A) i s t he f ood absorbed f rom a n i ndividual 's digestive syst em. Assimilation efficiency (A/G) is the proportion o f co ns umption (G) actuall y ab sorbed (Sushchenya 1969 , Odum 19 71, Wetzel 1975 ) . Although the t e rm A/G i s usua lly used in reference t o i ndividual o r ga ni sms , it also can be app lied to popu lations. Ege stion i s food that is not ass imi lated by the gu t a nd whi ch is elimina ted as feces (Pe nna k 1964 ). By co n t r ast , excretion is a waste product formed from assimilated f ood a nd gener a l ly i s e l imi nated in a d i s s o l ved form. 204 . Energy f low refe r s t o the assimilat ion of a population and i s de signated a s t he s um of produ cti on (P) and r espiration (R) , i .e ., A = P + R (Sus hchenya 1969 ; Odum 1971) . The e fficiency o f energy flow in a popul ation, p ~ R , may be approx ima tely e qua l t o the a ssimi l a ­ tion efficiency of an i nd i vidua l in t hat population (Sushchenya 1969) . However , since A/G o f t en de pends on age (Sch indler 1968, Waldbaue r 1968 , Winberg et al . 19 73 ,McDiffe tt 1970, Lawton 19 70 , Fisch er 19 72 , Pilarska 19 77b ) , t he A/G of an i ndividual may d i f f er significantly from t hat o f the population . Population A/G is essentially the mean A/G of t he i ndividuals co mposing the population a nd t herefore depends on the a ge -class s t r uc t u r e o f the population. At the communi t y level, the e f fi c i ency of e ne r gy flow t hrough t r oph i c webs ultimately influ­ e nces the r ate s o f fi s h produc tion and eutrop hication , both of which are important t o ma n . 205. The i mportance o f assimila t i on efficiencies in t he modeling o f z ooplan kt on and benthos i s pa r amoun t , pa rticu larly when mod e l s a pproa ch t r ophi c dynamics by way of feed ing equa t i ons . Assimilat i on efficiencies may be us ed in feedi ng equations to modif y co nsump tion and to yie l d the qua nti t y o f e ne r gy e nter i ng a n i ndividua l or popula­ tion . I n most models , a const a nt A;G va lue is used to modify cons ump­ t i on (e . g . 0 . 70 , Men shutkin a nd Umnov 19 70; 0 .70 , Umnov 1972;

105 0 . 57 . HacCormick et a l . 1972; 0 . 80 , Male 1973; 0. 70. S teele 1974; 0 . 20, Thoman n et a l . 1975; 0 .20 a nd 0 . 50, Scavia e t a l . 1976) . but i n o t he r model s A/G r a t i os were vari e d (e.g., 0 .50 t o 0 .76, DiToro et a l . 1971; 0 . 50 to 0 .70 , Ba ca et al . 1974 ; 0 .64 t o 0 .90, Ros s and Ni val 1976) . As s im ilat i o n wa s determi ned by t he d ifference i n consumpti on a nd the q uan tit y: excretion ( E) plu s eges tion (F), in mode ls by Zahorcak ( 1974) and Ha cCo rmi ck et al . ( 1974) . A potentia l d r awb a c k to t his met hod i s t ha t l i t erature data o n E and F a re relat i v ely scarce . Howe v e r . i f assimi l a tion efficiency a nd cons ump tion data are u s e d to esti mate E a nd F , a fairl y l arg e d a ta bas e i s a va ilable i n the literature . As simi l ation e fficienc i e s have be e n u s e d t o d e ter mine t he qua n t i t y o f ma tte r or ene r gy e n t e r i ng a de trita l pool from e ges t ion or e xcret ion (Me ns h utkin a nd Umnov 1970 , Patten et a1 . 1975, Swa r tzman a nd Bentley 1978 ). The d i f f erenc e i n consumption (i .e., whe n G ; 1) a nd A/G repres e nts t he f rac tion o f c ons ump t i o n tha t is egested a nd excreted. We ha v e used t h i s method to estimate E a nd F l os s e s from zoop lankton a nd benthos . 206 . Our approach to assimilation. egestion. and exc retion wa s t o tabulate A/G (Ap pend i x C) and to set up f reque ncy distributi ons of A/G F + E and G fo r po tential model compa r tme n t s (Figures 26-35) . I n doing s o, we hope d t o attain the l a r g e s t possible data base a nd determi ne t he d e g r ee of variation a mong v alue s within potent ial model compartmen ts . The f o llowi ng discussion prima r ily concerns a s s i milati on efficiencies F + E a nd factors i n f l uencing A/G . Be c a u s e A/G a nd ---G-- a re a dditive inve r s e . . A (F + E) funct10ns (1 .e. • G+ G ; 1), the discussion also i nd irectl y a pp l i es t o egestion a nd e x c r eti o n (i.e., a s A/G c h a nges in response ~ o e nv i r o nmen tal conditions, F ~ E a lso mus t exh i bit c ha nges tha t a r e o f e qual ma gni t ud e but o p posi te i n d i r e c tion) . Thus. Figu r es 26 and 27 a re F + E mirr or i mages o f Figures 34 and 35, r e spe cti v ely . Both AI G a nd ---G-- , f rom fre quenc y d i s tri buti ons , a re t o be us ed a s mul t i p l i c a t i ve modi f i e r s of consumption t o yield t he q uan tities of c a r bon a ssimilated a nd l o s t, respectively . 207 . Energy equations o f individuals or populatio ns are essential t o a t horough understandin g of assi mi l a t i on efficienc y . A c omplete

ene r gy equation may be e xpres sed a s : , , , ,

16 - ZOOPLANKTON f ~ ~ 12 ~ c- l- I- f- 4 f- - - o o 20 40 60 80 100 A/ G- x 100 Figure 26. Frequency hi stogram of zooplankton as similation va lues (A ) as a percentage o f cons umpt ion (C) . Based on da ta i n Appe ndix C ., -r- 16 c- BENTHOS

12 .- - ~ -- I- - - - r- 4 - - .-- l- I- o - o 20 40 60 80 100 A/G x 100

Figur e 2 7 . Frequency histogram of bentho s a s s i mi l a tion value s (A) a s a percen t age of cons um p t i o n (G) . Based on data i n Appendix C

10 7 G = p ( ) .. R + F + E (18 ) g + r +ev +s where G = consumption; P = produ ct i on, elemen ts o f whi ch are g rowt h (g) r epr oduction (e) . ex uv ia (ev) . a nd secretion ( s ) ; R = respirat ion ;F =egestion ; E =excretion . As similat i on eff iciencies ca n be estima ted . f h b . . . AP + R d A 1D two way s r om t e a S1 C e nergy equa l 10n . 1 . e . , G =~ a n G= G - F - E G 2 08 . In the l a s t t wo deca d es , radioac tive-is otope me t hods t h a t directly measur e upt a ke have been app lied (see App endix C f or a tabula­ tion of methods) . These met hods u s e radioisotope mov ements to e v a l uate e nergy pa r ame t e r s i n Equa t ion l B. Conove r ( 1966a ) devel ope d a n a s h­ rat io method t hat did not r equ i r e qu ant ita tive me a surement s o f G a nd F. Al l methods have techn ical probl ems , and results produced by t he various me t hods are o f t e n far from s i mi l a r ( Conover 1966a, St r e it 19 76, Pechen' ­ Finenko 1977) . To better unde r s t a nd why the assimilati on effi ciencies c i t e d i n the literature are so variable ( ca 2 t o 99 percent, Figures 26 and 2 7), we have e xamine d t he method s a nd environmental fact o rs whi ch influence them.

Methodology

209 .One o f t he e a r l i est methods was t.o ev a l ua te :

A P + R = (19 ) G G

Producti on ( P ) i n Equation 19 , o ften i s me a sured i n t e rms o f g rowth ( Pg ) (Czeczuga and Bobiatyns ka - Ks ok 19 72 , Fischer 19 72 , Trama 19 72 ) or per ­ haps as growth and exuvia l produ ction ( Pg + Pev)( Lasker 1966) o r as growt h and r eproduction (Pg + Pr) (Richman 1958 , Kryutchkova a nd Ryba k 1974, Duncan e t al . 19 74) . However, rarely are a ll componen ts of pro­ du ction, i nc l ud i ng e stimate s o f sec ret ion ( Ps) , determine d. 21 0. Secretion s l ost t o t he env i ronmen t during f eeding a nd up on egestion may c onst i t ut e a signifi cant portion o f producti on ( HcDi f fet t 1970) .Ot to (1975 ) e stimated Pg, Pev , and Ps i n larval Po tamopby l ax

108 c i ngulatus (Trichoptera) and found that Pe v and Ps constituted 16 . 3 perc ent ( 4. 1 a nd 12 . 2 pe r c ent , r e s pe ctiv e ly) of t o t a l production . Had he neglected t hese parameters, A/G would hav e been s i g nifi cantly und ere s t ima t e d . 2 11 . Potentia l err o rs i n t he esti mation of r espiration or con ­ s umption a re d i s c us s ed un der t heir respec t ive h e adings. I t i s s u f f icien t t o c on c l ude t ha t potential e rror s a re n ume rous, and the y a ll dec rease the acc uracy of A/G estimates . 21 2. When A/G is c a l c u l a t e d wi th thr ee independently dete rmined paramet e r s ( i .e., P , R , and G) , res e archers may e ncounter fairly h igh variat ion among r e sults. Th i s v a r i abili ty o f t e n r e s ults b e c a use ind e ­ pendent de termi natio ns of P , R, a n d G are conduct ed un der differe nt e xperi mental c on d i tions . Fo r e x a mp le , Comi ta ( 1964) e sti ma t e d the con s ump t i o n o f Di apt omus s ici loi des by meas u r ing c hanges i n the c on c e n ­ t r ati on of one f ood item ( Pa ndo r i na or Chlamydo monas) befo r e a n d aft er f e e d ing, in 5 0 ml o f pon d water . Re spira tion wa s d ete rmined in s ma ll , 2 - ml via ls whi c h con tai ned no a l ga e . P rod uction wa s esti mated b y e v a l ­ uati ng r e producti on (P r ) e xclusive ly . This estimation wa s made by c om­ put ing the d a i ly egg p r oduc t i o n o f fema l es t h a t we re col l ecte d f rom the f ield 8 ye a rs e arl i e r. 2 13 .The equation used t o c a l c ula t e a s similat i on e fficiency (Z i mm e r ma n e t a l . 19 75) i s :

A G - F - E (20) G G

Howeve r , mos t a u t hors omi t the e x c retion t erm [ E} , bec aus e it i s diffi cult to qua n t i fy a n d is s ome times con s i d e r e d negligible (La wton 19 70 , McDiffett 19 70, Da born 19 75 ,Sweeney a nd Schnack 19 77 ) . Techn ical l y , the f ollowing e q uati on mea sure s absor p tion effi c i ency (Ri c ke r 19 68) o r incor p oration (La sker 1960, Be ll a n d Ward 1970) a n d n ot assimi lation e f f i ciency :

(21)

109 214 . The e xcr e t i o n component (E) s ome t i me s appears t o b e i nsig­ nificant and probably c o u l d b e eliminated from assimilation e s t i ma t es . When Daphnia pulex swa llowed algae whole, it lost on l y 4 percent of its ingested c a rbon a s d iss olved o r g a nic car bon (DOC) ( La mper t 1978 ) . Ex­ c r e t ion by He xa genia l i mba t a wa s gene r al ly les s than 1 p erc ent o f c on­ s umption (Zimmenman e t al . 1975 ). 2 15 . I n con t r a s t , J o hann e s and Salomi (1967) f ound that Palaemonete s pugio (an estua r i ne decapod) lost DOC one t hird a s f a st a s i t c o n s ume d p artic ulate organic c a r bon (POC) . This e stimate i s p robab ly high, beca use some of t he DOC mea s ured undoubtedly was derived from food items ruptured d uring i ngestion (Conover 1966a) . Up to 17 per cen t o f t he a lga l c a r bo n fi l tered by Da phn i a pul e x was l o s t a s DO C from r uptured cel l s ( Lampert 1978) . Per haps t he best q uantitative approac h is to combine F a nd E a nd simp ly me a sur e a ll l o s s e s (Joh a n n es and Satomi 1967 ). Until mo r e r esea rch i s con d uct e d , researchers c a n not be c e r t a i n of t he magnitude o f e r ro r involved when E i s not evaluated . Apparently it varies among taxa. Fo r the purpo se o f thi s model, t h is potential ov e r est i ma tion o f A/G is co ns i dered a s part o f the random e rror affect­ ing all values. 2 16 . Qua n t i tative collect ion of f e ces, especia l l y from s mal l G - F - E zooplankton, i s pe rhaps the mo st seri o us problem with the G method . In macro be ntho s , however, t h e q uantitative col lection of feces i s not a l wa y s a p r oblem (Lawto n 1970 , HcDiffett 1970 ). Torn f e cal pellets and the subsequent l o s s o f f eces, as DOC or POC , u sually r esults in a n overestimation of AjG (Conover 19 6 4, 19 66 a ) . Th e situation is complicated by t he s u spen sion a nd rec onsumpti o n o f z ooplan kton feces . Coprophagy results in u nderestimates o f F and G and overe stimates of A/G (Co n over 1966a, S c hindler 196 8 ) . Unless p recautions are taken ( e.g . , s hor t feeding periods ), t hese e r r o rs c a n be v e r y significant . Though the loss o f f e c es i s t he most co mm o n sou rce of e r ro r , the col lectio n o f f oreign matter s uch a s algae, e x uvi a , bacteria, fungi, o r d etritu s with the fec e s , especia lly in prolonged e x per i me n ts , ma y r esu l t in a n u nd e r est i mation of A/G (C onov e r 19 6 2, 19 66b) . Lawton (1970) d i s cus s ed

1 10 in some detail the potential sources of error in determinations o f AIG by Equation 21. He concl u de d a s d id Cono v e r (1964) t hat most o f the potential errors t e n d to overestimate A/G . 2 17 . Sin ce p revious metho d s fa i l ed t o yiel d c ompa r a b l e resu l t s , Conover ( 1966a) d evelo ped a n a sh- r a tio metho d . Hi s me thod does not require qua n t itati ve c o l l e c t i on of f e c e s n o r measur e ment s o f c o nsumpt i on . The method is based on the assumption t ha t the inorganic Erec t.ton (ash ) o f ingested f oods is unaffected during gut passage .As s i mi l a t i o n ef­ f i c iency i s d efined a s

A F' • E' x 100 (22) G = (I-E ' ) (F') wh e r e F ' and E ' are t h e fractio ns o f o rganic matte r (i .e. • a s h-free d ry wt :dry wt ratio ) i n the i n gested f ood and feces . respectively . 21 8. P r us ( 19 7 1) , who calculated the A/G o f As ellus aquati cus G - F ( Isopoda) b y the ash·ratio and G me t ho d s , found that Asellus aquati cus excreted mi n e r a l s in e xcess dur i n g t he wint e r and a bsorbed t hem d u ring t he summe r . The d i f f e r e n t ial use o f mine r a ls by thi s spe cies t h us rend e r e d t h e ash - ratio metho d un r e liable ( P rus 19 71 ) . 2 19 . At on e t ime , the most promising me tho d s appea red t o be t ho s e in whi ch f o od s were labeled with radioisotopes o f pho spho rus (Hars ha ll and Or r 195 5 a, 19 56 ; Cohn 1958 ) o r c a r bon (Mon a kov a nd Sorokin 19 60, Sc hind l er 1968, Van note 19 69 ) . Using t h e s e methods, investigators c a n d i rec t l y mea sure the a c cum ulatio n o f isotopes i n t he body , excre ta , a n d feces of a n ani ma l , as we ll a s p rovide an esti mate of con s ump t i on . Though many variat ions e xist , the b a sic s t e ps o f t he method a r e a s fo llows : ( a) label f ood i tems a nd cor r e l a t e t h e radioac tivity, in co u n t s per minut.e (cpm) I to the c a lor ic value o f the f o od; ( b ) feed animals l abeled f o od ( p r e f e r a bly for a s hor t period o f lime so that defe cation a nd e xcretion o f iso t opes a re minimal) ; and ( c) feed animals unlabeled food un t i l a l l r a dio i s o t o pe s i n t he gut hav e bee n e liminated . By meas ur· i ng t he di f f e r ence in radioa ctivit y a c c umul a t e d in the b o dy of the a n i mal be f ore a nd after the e limi nation o f radioisotopes, a resea rche r c a n e stimate cons ump t ion a nd assimilation. respe c t ively. Radioactivity of

III the respired CO and f e ces provide s est ima tes o f E a n d f, r e spe ctive l y . 2 Thus, A/G can he ca l c u l a t e d by using the t erms A (cpm in t he body a n d CO o r ( cpm c o ns ume d minus c pm i n F a n d CO in t h e nume r a t o r , and G 2) 2) = (cpm consumed) or ( cpm in t he bo d y , F , a n d CO ) in t h e denominator . 2 2 2 0 . Radioisotope methods o f t e n are consi dered to be s ign ificantl y more a c curate than the o t her me thods o f d etermining A/ G ( Ma r s h a l l and Orr 1955b, Sorokin 1966 a , Pe chen' -Finenko 19 77 ) . The basis fo r thi s be l i e f is that radiois otope moveme n t s into a n anima l cons t i t u te t he o n ly d i r e c t meas urements o f cons umption and assimilation . By contrast, a number of r e searchers s e rio us l y que sti on the va lue o f most t r a cer s t ud ies cond uct e d to d a t e . 221. Joh a n nes and Satomi (1967) s t a t e d that most A/G values de­ termined by r adi o carbon me t ho d s are ove r estima t es . Overes timat es res ult from l osses o f u nla bele d ma t e r i a l s from t he gut wa l l t o the gut lumen . Unle s s t h e worker i s absolutely s ure t hat n o 14C is e xc r e ted , respired , or l ost t o the env i r onment, the expe riment is un i n terp r e table witho ut d eta iled i nfo rma tion o n r eacti on k ineti c s ( Conov e r a nd f r a n c i s 1973 ) .

Lampert ( 1975) d e monst r a ted that 14C l o sses ( i .e. , a s 14C0 2 ) c a n be a c curately measured o n l y du ring f e eding experiments . Ca r bon losses as 14 CO usually are negligible whe n me a sur e d at the end of feeding perio ds 2 (Sch i n d l e r 19 6 8 , Kibby 19 71 b ); h owe ver, i n Daphnia pulex monitored d u r i n g f e e d i ng, 14C l osses were a bout l a , 20, and 30 percen t o f a s ­ similated carbon i n 10 - , 60 ~, and 300- min experimen t s , respe ctively ( Lamper t 19 75 ) . Unmon i tored l o sses o f t hi s ma gnitude r e s u lt i n signi f ­ 14 i cant overestima tes o f A/G . Lamperl ( 19 75 ) d eveloped a mo d el o f C l o s s f or Da p hn i a pulex. 222 . Some o f the a s sumptions o n wh i ch the i s o t ope met hods a re based a pparently a re i nvalid . Fo r e Kamp le , t h e s pecimen i s a s sumed l o be a single c ompa r t me n t s ystem in wh i c h the r e is i nstan t a neo us a nd c om- plete mixing o f l a be l e d and unlabeled c ompo u nds . I n addition, l a be l e d c ompou n d s are supposedly evenly distributed a nd d o not recycle . Unfor­ tunate ly, seve r a l pools o f ca r bon and p hosp ho r us wi l h d i f feren t turnover rate s hav e be en demons trated a n d trdc e r recycl i ng d oe s occur (Conov e r 19 6 4, Co nover and Francis 19 73. Lampert 19 75 ). Co nove r ( 196 1)

11 2 r e cognized two pho sphoru s pools in Ca l a nus finmarchicus. a nd Lampert ( 19 75) s t a t e d that Daphnia p ulex was not a sing le c ompa r t me n t syst e m. Cono ve r and F r a n c i s ( 1973). who developed a multi compartment model t o accoun t f o r trac e r r e cycling among compa r t men ts . s t a t e d . Unless it is known that no r e cycling o f i s otope h a s o c c u r ­ red, the assumption of line ar uptake . when i n fact the sys ­ tem i s not linear. even f or s hor t periods , can l e a d t o s igni f ican t e r r o rs in the e sti mation of inge s t i on or fee ding.

223 . I n s umm a r y , no ne o f t he me tho d s of assessi ng a s similation. e gestion , a nd excretio n are invaria b ly f o olproof. but o ne me t h od may be signifi can t ly mo r e a c curate than ano the r f o r a particular s pe c i es or u nd er s pecifi c e xperime n t a l cond i t ions . Although assimi lation eff ici e n ­ c i es have be e n cal culat ed f or many animals ( Appendi x C) , many o f the estimates are probably o f l i mited value . Variation i n e xp e r i me n t a l results i s a f unc t ion o f a mul t i t ude o f fa ctors. b ut maj o r dis crepancies prob a b l y ~ e s u l t from vari a ble expe riment al c o nd i t i o ns ( Ma rsh a ll 1973 ) . Apa rt f r om va r i a t i on amo n g s pecies. age groups , and sex , f a cto r s s uch as t e mperatu re , l i gh t. containe r size , anima l density, animal size. a nd qua lity o f f oo d al l exer t a marked inf luence on e xpe r imental r e s ults (Marsha ll 19 73 ). Thus , metho dol ogy is n o t the o n l y c ause of vari a bility i n Aj G e s timate s .

Factors Affecting As s imi l ati o n Efficien c y

Food type 224 . Undoubtedly t he most s ignif i can t f a ctor aff e cting a s simi la­ t i on e f f ici e ncy i s f o od type . The e f f e ct i s not v e r y ap parent i n ca r n i v o r e s , l ike the o do n a t e Pyrrho s oma nymphul a (La wton 19 70 ), t he p l e copter a n Acro neuri a ca lif o r n i c a ( Heiman a n d Knight 19 75 ) . and the amphipod Ca l l iopius l a e v ius culus (Dagg 19 76 ;Append ix C) . be cau s e the f ood type , energy con ten t . a nd d i ge stibility o f animal f o ods do not vary great l y . For example . mos t bent hic c a r n i v o r e s have Aj G r ati o s between 0 . 80 a nd 0 . 9 5 (Figure 28). By con l rast , ranges i n Aj G a re wide in herbivo r e - detritivores (Figu r e 29) because these a n imals o f ten c onsume f oods o f varyi ng e nergy con ten t a n d digest ibi l ity -- e .g., the

113 16 BENTHIC CARNIVORES ... 12

r-r--: 8 - I- 4 ~ I-- o I o 20 40 60 80 100 A/G x 100

F igure 28 . Frequency h i sto g ram o f b e nthi c carnivore assimi la t ion v alue s ( A) as a percentage o f consumption (G) . Based o n data i n AppendiX C

16 r-r-: BENTItIC HERBIVORE. - DETRITIVORES

12

8 r-r- I-- I-- e- I-- - I- ~ 4 ~ r- l- I- o Ih o 20 40 6 0 80 100 AIr> x 100 F i g ur e 29. Frequency h isto g ram of bent hic berb ivo r e -de t r i tiv o re assimilation v alue s (A) a s a pe r c enta g e of consump tion (G) . Based on data in Appendix C

114 c l a doceran s Da p h n i a l ong i s p ina ( Schindle r 19 71 ) and Sid a c rys t a ll i na ( Mona kov and Sor o ki n 19 72) and t he a mphipod Ga rnm aru s ps e udo l i mnae us ( Ha rlache r a n d Kendr i c k 19 75 ) . 22 5. Many workers have cor r e l a t e d A/G with t h e c a lor ic value o f foods (Odurn 19 71 , Wetzel 19 75) . Schindler (1968) f o un d that t he assi mi ­ l a t ion e fficien cy o f Daphnia magna increased from a bout 10 t o 9 9 pe r c e n t a s t he c a l o r i c content o f i t s d iet increased f r om 1.3 to 5.3 c a l o r ies/mg dry we i ght . Th ereafter, fur t her increases i n c a lor ic value r esu lte d in decreasiag A/G--per haps due to decrease d d igestibi l ity o f these f oods . S i mila r co r r e l a t i on s have been c i t e d fo r p lanktonic c r us t a c e a n s ( Pechen ' -Fi nen ko 19 71 ) a n d suggested for Asellus s p. and Gammarus s p . ( Swiss a nd J oh nston 19 76 ). 226 . Assimi lation e f f i ciencies also depend d i r e c t l y upon t h e q uality and d i ge stibi l i t y of f oods (McDiff e t t 19 70, Fischer 19 70 . Odum 19 7 1 , Wetz el 1975 ) a nd apparently are i nvers e l y related t o the ash con­ t ent (Co no ver 1966 a , Schindler 19 6 8 ) . By c ont r a s t ,La wt on (19 70 ) found t h a t t he A/ G o f Py r rhosoma nymp h u la was not c o r rel a t e d t o a s h co ntent nor to c a l o r ic c ont e n t . 22 7 . I n ge nera l , t he A/G o f ani mals fed liVing or senesce n t p lant matter i s les s than that o f animals fed l i Ving or d ead a n i ma l ti s s ue (Sushchenya 19 6 9 . Monakov 19 72 , Monakov and Sorokin 1972) . This o bs e r ­ vation wa s substantiated by most o f the l iterature values for be nthi c c a r n i v o res and he r b i v ore-det r i t i v o r e s ( cf F i gu r e s 28 a nd 29 ) . Certain phy t op lankte rs) howe v e r , ma y be a s s imilated v e ry efficie n tly b y zooplan k­ t on ( e . g . , see Schindler 19 7 1. Monakov and Sorok in 19 72 , lla yward and Gal lup 19 76) . Diges tibi lity i s probably more related to the high caloric a nd l ow cel l ulo s e c o n t e n t s of s ome phytoplankters t h a n t o increased efficien cy o f d igestion by z o op lankton . We s e parated z ooplankton assi mi­ l a t i on effic iencies o n t h e basis of d i e t . Blue-gre e n a lgae a nd detritus a r e apparent l y assimilated l e s s efficie ntly t han are green algae (F i g ­ ure s 36 and 3 7, r e spectively) . Th e data for t he assimilation of g reen a lgae a re h ighly variable, pe rha p s r eflecting the tremendous diversity o f s t r uc t u r e wi thi n the Ch lorop hy t a . 228. Though the us e of de t r i t us and/or microflora as food by

115 hen t ho s is wi d ely accepte d (Cummins e t al . 19 66, Hyne s 19 70 , F i s h e r a nd Lik ens 19 72, Ma r z olf 19 6 4, Barloc he r and Ke ndri ck 19 75, Rod i na 196 6 ), t he us e o f the s e items b y zoop lankt o n is n o t generally a cknowledged . I II mo s t mode l s, zoop l a n kt o n a nd bentho s d epend p rimari ly upon phytoplan kt on a s a food sou rce . Th is b a s i c pre mi s e probably is inac c urate f or res er­ v o ir bentho s a n d zooplan k t on . A d e t a i l e d d i s c us s i o n o f t his top ic wa s g i ven i n t h e sect.ion "Detrit us a nd Microf lora a s Fo od" in Pa rt I II o f t.h is repor t , page 53 . Fo od con cen t.ration and f eeding r ate 229 . Assimila t.ion efficiencie s h a v e be e n o bs e r v e d t.o d e c r e ase significant. ly wit.h increa sing f o od c oncentr a t i o n o r rat.ion in f ilt.e r­ f e eding zoop l ank ton, e .g. , Dap h n i a magna (Ry t he r 19 5 4 , Schindler 196 8 ) , Da p hni a p ulex ( Richman 195 8 ) , Brachionus pil c a t i l i s (Doohan 19 7 3 ), Diap t omus g raci l o i des ( Kr y utchkova and Ry bak 1974) , a nd seven species o f Entomo s t r a c a (Wi n be rg e t. a I. 1973 ) . The s a me t rend als o h a s been o b­ served in other a n i ma ls s uch a s the n ema t o de Plec t u s palu stris (Du nca n et a l . 19 74 ), the gas t r opod Gon iobas is c l a va e f o r mis ( Elwoo d and Gold st.ein 19 75 ), a nd various Cr us tacea ( S ushchen ya 1969) . Th e a bove findin g s s eem to s u pp o r t t he the ory o f s up e r f l u ous f e e d ing ( Harvey et a l . 19 35 , Bekl e mi s he v 19 6 2 ), wh i c h hold s t hat a nimals ass i mi late f o o d most e f f i ­ c ien t l y wh e n it i s pres ent in sma l l quantitie s . Wh e n f o od i s a b un d a n t a nd c o ns ump t i o n exceeds the ani mal' s f o od req uireme nt , t he e f f i c ien cy o f digesti on d e c r e a s e s be caus e of t h e a n i mal' s i na bilit y l o e f fici e n tly pro c e s s t h e large quantities of food . In fi l t er- feeding Cl a d o cer a , Copepoda , and perhap s Rota t oria, fi l tra tion rates c a nn o t be r educe d e nou gh t o l imit the intake o f food , whe n the food i s pre s ent at v e ry h i gh concen t r a t i o ns . Under the s e con d i t i ons e x t r a o r s uperfluo us f eed­ ing can o c cur (Mon a kov a nd So rokin 1961 , a s c i t e d b y Mo nakov 19 72 ) . F i eld obser v a t ions a lso seem t o substantiate s uper f l uous f eed i n g . King ( 1967) noted that undi ge ste d a l g ae appear ed i n t h e fec es o f the r ot.i f er Eu c hlanus d i l itata o n ly when t h e a lgae were p r e s e n t a t very hig h concen ­ t r a t i o ns. A s i mi l a r ob ser v a tio n also wa s ma de for Da p hnia ma gna ( Ryth e r 1954 ) .

116 230. Some authors ha v e ob served consta n t A/G with increasing f ood concen t ration a n d the r efore disagree with the theory o f s up erf l uous f e edin g . Pechen ' -Finenko ( 1973) noted that i n raptoria l z oop lankters (mos t ly p red a tors) ,A/G r emains const a n t over a wide r ange i n foo d c on ­ c e n tra tion. P resuma bly, thes e t ypes o f ani mals c a n regulate c ons ump t ion a nd therefore o p t i mi ze A/G. Pyrrhosoma ny mphu l a, a c a r n i vor o u s o do na te (Lawto n 19 70), and Neanthes v irens, a c a r n i v o r o us p olychae te (Kay and Brafi eld 19 7 2 ), a lso e x h i bit fairly uniform A/G r egardl ess o f the quan­ tity of f ood consumed . Even t he fi lte r - fee d i n g copepods Diaptomus g r aci l is ( Kibby 19 71b) a n d Calanus hyperboreus (Conover 1964 , 1966a ) exhibit fairl y u niform a ssimilati on effi c iencies (64 .2 t o 68 .4 perc ent and 39 .6 to 7 1 . 1 percent, respe c tively) when food con c e n t ra t i ons are vari e d s ign i f i cantl y . 23 1. Pechen' -Finenko ( 1973 ) argued t hat the c o nce ntr a t i on at wh i ch s uper f l uo us feeding o ccu rs e xce eds t h e c oncentrations o f f o od found i n na t u r e . I n a dd i tio n, he suggeste d that automatic f ilter feeder s can regula te ass i mi l a t i o n by altering their f iltration ra t e and A/G . Pe chen '-Fi nenko ( 19 7 7) expressed the belief that the a p pa rent dis- c repancies i n pre vious r e s u lts o f experiments on food conce n tra tion were entire l y due t o v a r iatio ns in me t hod olo gy . Fo r example, he v iewed the downward trend i n the A/G o f Daphni a pulex (Richman 195 8 ) a s an a rtifa ct g ene rated by Ri chman's us e o f the t ~ R me thod . However , Sch i n d ler ( 1968) a nd Ha ywa r d and Ga llup (19 76 ), usi n g radi o carbon techniques , also obser ved decreasi n g A/G a s f ood c o ncen t r a tio ns we r e increased .S ch i n d l e r ( 1971 ) bel i eve d that s up e rfl uo us feeding may be come evide nt on ly when z ooplankton a re f eeding on c ert a i n type s o f food . He concl ud e d t hat a ssimilation efficiency varie s inversely with t he inge stion rat e , when diff ere nt f oods a r e co ns ume d . 232 . Firm c onclus i ons c a n not be made regarding t he relation of assi milation e f f ici e ncy t o foo d c onc entration. Lawton ( 1970) noted t hat the A/G o f Pyrrhosoma nymphula may increase, decrease, or r ema in con­ s t a n t a s f e e d i ng rates i ncr e a s e .He s uggest e d that all three responses are possible i n nature. Hayward and Gallup (1976) pointed out t hat the situat i on i s even more c omp lica t e d t h a n mos t pe op l e believe. Ac cording

11 7 to t heir work , A/G is a function o f f ood concen t r a t ion, but thi s func­ tion vari es wi th t emperature . They s t resse d t he need f or multi variate i n fo r mat ion on a s s imilation a nd sugge ste d that grea t ca r e be exerc i s ed in the i nterpretati on of r e sults . 233 . Pra c t i cally a l l mod els we r e viewed us ed gr azing c onst r uc ts t hat we re dependent on f ood dens i t y . I n ot her words , t he s e authors be l i eved tha t a s similati on e f f i ciency r ema ins const a nt at a l l food con­ ce n t r a t ions , where a s cons umpt ion cha nge s a t l ow t o moderate food conce n­ t r a t i ons . This premise may o r ma y not be co r r e c t , but i t i s practi cal in that the e f f e cts of co ncen t r a t ion on g razing are eas ier t o examin e a nd s imulat e than are thos e s ame e f fect s on assimilation e f f ici ency . DiToro e t a l . (1 9 71) used a density i ndepe nde nt (i .e ., l i ne ar) grazing r e l ationship ba s ed on the i dea of s uper f l uou s f e eding and made a s s imi­ l ation efficiencies vary with food conce ntra t ion . The r ela t i on o f f eeding rate t o food conce nt r a t ion i s ess entially linear ove r mos t foo d co ncen t r a t i ons a nd though a linear f un cti on may be appr opria t e i n most cases, d i f fi culti e s i n dete rmini ng the e xa c t effe ct o f f ood concent ra­ t i on on as simil ation e f f i c i enc i e s r ender thi s a ppr oa ch les s appealing . Tempe r ature 234 . Cha nges i n A/G have be en pos i t i ve l y co r r e l a t ed with water tempe rat ure fo r Cladocer a (Webb and J ohanne s 1967, Sc hi nd l e r 1968, Haywa rd a nd Ga l l up 19 76 ), Cope po ds (Conover 1962), va riou s C r u~ t acea (S ushchenya 19 69 , Pe chen' -Finen ko 1971) , Insecta (Hei ma n and Knight 19 75 , Ot t o 1975 ), and Gas t ropoda (E l wood and Golds t ein 19 75 ) . Effects o f temperature on metabo l i sm ha ve bee n de s c ribed by the Q law (Prosser 10 a nd Brown 1961 ), whi ch s t a t e s that ectot her m metabolism increas e s two t o t h r e e t ime s with a 10° increas e in temperature . Unde r i deal cond i t i ons, A/ G s ho ul d be l ow a t l ow t e mpera tur e s, i ncrease t o a maximum a s t empera­ tur e i ncreases to a species-speci f ic opt i mum , and g r a dua l ly de c l i ne as t empera ture approaches the upp er t olerance l imit fo r t he s peci es . 235 . Unfo rtunately, t he ideal rela tionship o f A/G t o t empe r a ture is no t a l ways ob s erved . The A/ G of Ca lanu s hyperboreus (Conover 1962 ), betwee n 2° and 11°C, d i d not vary s i gni f i can t l y (64 . 5 t o 68 . 0 percent ) . In the ga s tropod Goniobasis c lavaefo rmis A/G r ema i ne d co nst an t between

118 10° and 20 °C (El~ood and Gol dst e i n 1975) . As similation e fficienc y a l so was unaffected by temperature in a number of o t he r animals (Lawton 1971, Kibby 1971b , Dagg 19 76). 236 . A po ssible e xplana t ion for these dis crepancies in published data is that t emperature not onl y affects P and R but also con sumption ( G) thr ough the effe cts of fo od concent r a t i on and temperature on fi l t r a~ tion rates (Hayward and Gal l up 1976). There is a good po s sibility that increased t emperature, within a ce r t a i n range, ma y not increase the A/G of an organism . This response could occur if the increas e in a s simila­ t ion (P + R) was matched by a concomitant increa s e in consump t ion (G a l s o increase s wi th t empera t ure; see " Eff ects of Temper ature on Consump­ tion" i n Part I II of this report, page 66) . In sho r t , s ever a l va riable s are interrelated and the fina l r esult may ha ve emer ge nt properties ( i .e., propertie s t hat canno t be p redi c t ed by s epara t e l y exami ni ng the e f f ects of the individual variables) . Anima l deve l opment 237 . As similation efficiencies have be en observe d to change s i g ~ nifi cantly a s a ni ma ls devel op . Wh ether this r esult is a f unc tion o f age o r wei ght i s not certain, but , in s ome organisms at least, the cha nge i s c l ear ly r e lated to l i fe history events s uc h a s metamorphosis (Fi s cher 1966 ) . Hany o rganisms change thei r diet during deve l opment (e.g., na uplii of predaceo us capepods oft en are he r bivorous un ti l they r each a ce r t a i n size) . Because f ood type probably is t he most s i gni fica nt fa c­ tor influencing assimilation e fficienc y , cha nges in diet during the cour se of development may s i gni f icant l y alter A/G r atios (Sc hi ndl e r 1968, Wa ldbaue r 1968 ). 238 . Assimilation e f f icienc ies have been observe d to decrease, remain co nstant , or even increase dur ing the deve l opment of va r ious aquatic invertebrates . Decreasing A/G ratios during development were not ed i n the zoopl ankt ers Daphn ia magna (Schi ndl e r 1968 ) and Macrocyclops a lbi dus (S hushki na et al. 1968 ), and i n the insects Pyrrhosoma nymphula (Lawton 1970 ), Pte r onarcys s co tti (HcDiffett 1970 ), Hedri odiscu s t r uquii (Stockne r 1971 ), and Leste s spansa (Fische r 1972). However, a ssi mi l a t ion e f fici enc ies rema ined co nst ant during the deve lopment of the copepod

119 Macro cyclops albidus ( Kl e kows k i and Sh u s h k i n a 1966b ). the mollus c Dre iss ena polymorpha (Monakov 19 72 ) , the amph ipods Gamma rus pulex (Nilsson 1974), a nd Ca l l i op i us l a e v i us c u l u s ( Da g g 19 76). Brachionus rubens (Rotatoria) e x h i b ited i ncreased A/G during development (Pilarska 1977b), a nd Lawton (1970) believed that the A/G of Pyrrhos o ma nymphul a (Odonata) cou l d i ncrease , decrease, or r e main c o ns t a n t under a g iven set of environmental c o nd i t i o ns . Reproductive state 239 . Few data a r e available that d e s c r i b e the effects o f an animal' s reproductive s t a t e on assimilation effi c iency . Daphnia ma gna a n d Q. sch o d l e r i be a r i ng eggs or embryos a ssimilate at a hig her rate than nonovigero us f emales (Schindler 19 68, Ha ywa r d a nd Ga l l up 1976). Th e assimilation efficiency of Asse llus aquatic us varied from 26 t o 44 percent depending on reproductive c o nd i tio n , sex . and populati o n d ensity (Prus 1976 ) .

Summary o f Co ns t r ucts

240. First. users should sel e c t the f requency h i stogram (Fi g ­ ures 2 6 -33 . 36 , and 3 7 ) t hat best describes t he mode l compa r t men t t hey are consi d e r i ng. Secon d , the f r eque n cy histogr am s hou l d be transformed into a probability d i str i but i o n of A/G ratios ( r estr ict e d by the c on ­ f i d e nce limits placed on t h e p r ob a b i l i t y d i stribution by the us er), a nd a range of A/G ratios s houl d be s e lected . Third, c o ns ump t i on (mg ca r bon . - ] -} mg c a r bon -day ) --generated by grazin g cons t r u c ts i n Part II I- -shouid be mu l t i p l i e d by the s e lect e d A/G r atios, a c cordi ng to Equation 1 . The r esulting products des c ribe the range o f weight-spe c ifi c assi mi l atio n - 1 -1 (mg ca rbon -mg carbon -day ) by the c ompa r t me n t . To de t ermi ne t he r ange -1 of weight- specific l o ss (ege stion + excretio n--mg c a r bo n -mg c arbon -1 - day ), use rs s houl d s ubtr act A/G rati o s from one and multiply weigh t - spe cific c o nsump tion by t h e res ulting d i f ference . Th e product of t he we ight-specific r a t e s of assimilation o r e ges t i o n + excretion ( as de­ termined ab ove ) and the b i omass of t he model compa r t men t (mg c a r bon ) yie l ds t he weight of c a r bo n a ss i mi l a ted or lost. r espe ctiv e ly .

120 24 1. Because t he distr i bution of A/G values for cladoce r ans (Figure 32) was essentially uniform, we recommend that zoopl ankt on be considered as a single compar t ment (Figure 26) .However , when greater resolution is r equ i r ed , the frequen cy histograms of rotifer and copepod A/G (Figures 30 and 31. r es pecti ve ly) may be used , but cl adoceran A/G r atios s hou l d be r andomly selected f rom a range of 0.05 to 0.55. Bio­ mass of zooplankton s houl d be arbitrarily assigned a s follows : Cl ad ocera = 60 pe rcent, Copepoda = 35 pe r cent, Rotatoria = 5 pe r cent , unl e ss more accurate dat a a r e ava i lab le. Rot atoria assi mi lation. for example , may be calculated as O.OSh [G(A/ G)], where b = t otal zooplank­ ton biomass (mg carbon), G =zooplankton consumption (mg carbon·mg - 1 - 1 ca rbon · day ) , and A/G = Rotatoria assimilation efficiency (from Figure 30) . 242 . Bent hos s hould be compartmental ized int o ca r nivores and herbivores- de t ritivo res on t he basis of thei r respective assimilation efficiencies (F i gures 28 and 29). Bas ed on the ecol ogi ca l growth ef­ f i ciencies of a nemat ode (Dunc an et a l. 1974), a chi r onomid (Kajak and Dusoge 1970) , and an oligochae te ( lvlev 1939), we be lieve that carnivores should cons t i t ut e 20 ± 10 percent of t otal benthi c biomass , when the benthos compartment is divided . Assimilation by benthic herbivores­ detritivores may be calculated as 0 .80b [G(A/G)I] and that of benthic carnivores as D.20b [G(A/G)2 ]' where b = total benthic biomass (mg - 1 -1 ca r bon), G = benthos cons umpt ion (mg ca r bon·mg ca rbon ·day ). (A/G)} = A/G ratio f or herbivore-det r i t i vores (F igure 29), and (A/G)2 = A/G rat i o for ca r ni vores (Figur e 28) .

Conclusions

243 . Ass imilation efficiencies are i mpor t ant i n biological models because they can be used to modify cons umpt i on and thereby yield t he rate of ene r gy flow into model compartments . Egestion (F) and excretion (E). which technically differ, a r e de fined as a s i ngle l os s in the mode l --the additive inverse of assimi l ation efficiency (A/G + (F ~ E) = 1) . 244 . Because methods empl oyed to estimate A/G are inaccu r ate, we

121 8 ROTATORIA

6

r-t-

2 - - e-

o I n n n o 20 40 60 80 100 A/ G- x 100 Figure 30 . Frequency hi stogram of Ro t at or ia as s imilation va lues (A) as a pe rc entage of consumption (G) . Bas ed on da t a i n Appendix C

8 r- COPEPODA

6 - - r-t- - - r-t- - l- f- 2 f-

o I r o 20 40 60 80 100 A/ G x 100

Figure 31 . Fr equ e ncy h i s t o gram o f Copepoda ass i mi l a t i o n value s (A) a s a pe r c e nt a g e of consump t ion eG) . Bas ed on data in Appendix C

122 ,, ,, 16 ,,, ,

CLADOCERA f 12 I

~ ~ ~ ~ l- I- ~ 4 l- I- ~

~- l- o I I-- o 20 40 60 80 100 A/G x 100 Figure 32. Frequency histogram of Cladocera ass i milation values (A) as a percentage of consumption (G) . Based on da ta in Ap pendix C

16 c-

ENTOMOSTRACA

12 ~

- ~ l- I- f-- l- I- 4 l-

I- '-- o o 20 40 60 80 100 A/G x 100 Figure 33 . Fr equency histogram of Ent omostraca assimilat ion va2. ue s (A) as a percent age of co nsumpt i on (G) . Based on da ta i n ,Appendi x C

123 16 - ZOOPLANKTON

- r- 12 I- - - 8 r- r-

4 I-- - - o o 20 40 60 80 100 (E+FJ !G x 100 Figur e 34 . Freque ncy h i s t o g r am o f zooplankto n e gest i o n ( F) a nd excre tion ( E) v alue s a s a percen tage o f c onsum p tion (G) . Bas e d o n data in Append i x C

16 - BEN nIOS

12

r- r- ~ r- I - - r- - - - - 4 ~ I-- - I-- ~ o o 20 40 60 BO 100 (E+FJ ! G x 100 Figu re 35 . Frequency hi s togram of bentho s eges t ion (F) a nd e xcr etion (E) v alue s a s a pe r centag e o f c onsump t ion (G ) . Based on data in Appendi x C

124 12 BLUE·GREEN ALGAE AND/OR DETRITUS AS FOOD

4

o o 20 40 60 80 100 A/G x 100 Figure 36 . Frequency histogram of assimilation values (A) as a percentage of consumption (G) when zooplankton were fed blue­ green algae and/or detritus

GREEN ALGAE AS FOOD 12 f

4

o o 1Il 40 60 80 100 A/G x 100 Figure 37. Frequency histogram of assimilation values (A) as a percentage of consumption (G) when zooplankton were fed green algae

125 d id not devel op cons tru c ts t o predict c ause-ef fec t r el a tions betwe en A/ G a n d facto r s s uch as f ood c o ncen t ration , t emperature. a nima l d evelopment . o r r epro duc t ive s tate. When s i mi lar methods were u s e d . food t ype gen ­ e ra l ly was t he mo s t i mpo r t a n t factor a ffect ing A/G (cf Figu res 28-29 and 36-37) , but food c on c e n t r a t i o n a n d temperat u re e ffe cts were inconsistent . Few dat a tha t i l l us t ra t e the effects o f rep roduct ive s tate o r animal development have been publi shed.

126