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Factors involved in herbivore food preference
J. <‘_v,j.nx,r. Biol. ~col.. 1980. Vol. 42, pp. 13-26 0 Elscvier’North-Holland Biomedical Press
FACTORS
INVOLVED
IN HERBIVORE
FOOD
PREFERENCE’
Abstract: Herbivore food preference can be measured etther in terms of attractivcnesb or of edibllit) : these quantitlcs are not necessarily correlated. The isopod I~/o/ctr h~//ic~o (Pallas) is attracted to large. tough. branched algae (perennials) while the amphipod .Anlpirhoc~ ~rliclrr (Smith) is attracted to softer. filamentous or bladed algae (ephemerals). Attractivenchs for Anz~~irhoc~is related to the nutritive value ofthe algae; this is not so for I~lot~. which responds more to algal morphology and availability. /t/~rctr‘\ mobility. possible susceptibility to fish predation. and prcfcrcnce for moderate v,a\c‘ eupo\ures mnq select for a primary response to alpac as habitat rather than as food source.
Herbivore food preferences are of considerable theoretical and practical interest to ecologists. Preference determines the quantity and quality of food ingested by a grazer and hence affects its physiological condition and fitness (Hsiao & Fraenkel. 1968). Herbivore preference also interacts with plant competitive abilities, life hiatories. and physical tolerances to determine the impact of a grazer on the plant community (Lubchenco, 1978). Frequently, herbivore effects on plant distributions. biomass, and diversity are dramatic (Huffaker & Kennett, 1959; Harper, 1969; Paine & Vadas. 1969a; Mann & Breen. 1972; Janzen. 1973; Mattson & Addy, 1975; McNaughton, 1976; Snyder & Janke, 1976). Furthermore. the relationship between plants and herbivores is not static; each may effect evolutionary change in the other (Ehrlich & Raven, 1964; Dethier. 1970; Dolinger c’t 01.. 1973: Freeland & Janzer~. 1974; Gilbert. 1975; Benson CI [I/.. 1976; Edmunds & Alstad. 1978). Two distinct components of food preference are commonly recognized: one relnting to the selection of a potential prey item (attractiveness). and the other relating to the rate at which that prey is ingested (edibility). Attractiveness is measured by methods that permit herbivores to choose betbeen several possible foods. This may involve chemoreception over some distance (Vadas. 1977) or it may involve direct chemical and tactile sampling of plants (Himmelman & Carcfoot, 1975: Lawrence. 1975: Lubchenco. 1978). Methods dealing with edibility assume that. under equivalent hunger conditions, herbivores consume preferred items faster (Leighton & Boolootian. 1963: Carefoot, 1967); edibility will retlect not only the speed with which a given item satisfies the physiological needs of a herbivore, but also the ease
M. E. NIC’OTRI
14
with which that item is handled edibility
have sometimes
are distinct
and measure
and ingested.
In the literature,
been used interchangeably; different
aspects of preference
Preference may be influenced by factors not relating ties of the plant. For instance, small aquatic herbivores
however,
attracti~~encss
and
it is clear that they
(Lawrence,
1975).
directly to nutritional qualithat live nestled among algnl
fronds may utilizean alga as habitat as well as food source. The amount of protection offered from predators or the amount of shelter from wave action are irnport~~t~t habitat characteristics (Colman, 1940; Wieser. 1952; Nagle, 1968) and might influence herbivore choice as much as the food value of the plant. The predictability of plant presence in space and time is also important and, in evolutionary terms, may affect herbivore preferences (Paine & Vadas, lY6Ya: Feeny, 1976). Preference has been studied in a number of marine herbivores. Investigators generally have concentrated on sea urchins (extensively reviewed by Lawrence, 1975; Vadas, 1977). molluscs (Leighton & Boolootian, 1963: Dahl, 1964; Leighton. 1960: Carefoot, 1967; Himmelman & Carefoot, 1975; Nicotri. lY77a; Lubchenco. lY78). and fish (Tsuda & Bryan, 1973; Vine, 1974; Ogden, lY76: Ogden & Lobcl. lY78). There is some illformat~on available about the diets of noi~plankt~~nic ~lerbivor~~~ls crustaceans (Ravanko, 1969; Jones, 1971; Carefoot, 1973). but, in general, pref’crences of this grou’p are poorly known. This is unfortunate since such crustaceans are common and often quite abundant. This study was designed to examine the food preferences of two of these crustaceans, the isopod Ihtcm hrrlticn (Pallas) and the amphipod ,~~~irlz~~~~wlidu (Smith). After factors that influence both components of preference have been investigated. results of this study are compared with preferences of the periwinkle Littorirra littolwr. an extremely common and abundant marine gastropod studied by Lubchenco (1978). Since the distribution of Littori/rt/ broadly overlaps that of I&~M and Anpith and all three grazers could potentially be using the same plants, it is of interest to compare the similarity of t’ood preferences. I&~LJLIholticu is an active isopod found among seaweeds in intertidal and very shallow subtidal zones throughout temperate latitudes (Naylor. 1Y55a). It is herbivorous (Naylor, 1955b; Ruvanko. 1969) and is an extremely abundant potential pest in a polyspecies aquaculture system at Woods Hole Oceanographic Institution. Cape Cod. ~ass~~chusetts (Ryther of (I/.. 1975: Nicotri, IY77b). it is also an opportunistic scavenger (Sywula, 1964) and is cannabalistic at high densities. It grolvs on available food. and may reach sizes of 3 cm fast, up to 2 mm/week, depending (Nicotri, 1977b). A7~7pir/7~w IU/~&I is a sedentary tube-dwelling amphipod, rarely leaving its tube except under duress (Skutch, 1926). It may reach very high local densities (Bousficld, 1973) and often does so in the aquaculture system at Woods Hole (Nicotri. 1977b). Since movement is limited and the alga chosen becomes both habitat and rood source, initial settlement is quite important. However, under adverse conditions. individuals can and do move and are capable of swimming rapidly for short periods.
HERBIVORE
Growth maximal
averages
about
I mm/week
body length is about
under
conditions
I .8 cm (Nicotri,
MATERIALS
15
FOOD PREFERENCE
AND
of optimal
food a~~il~~bilit~ :
1977b).
METHODS
Eighteen species of marine plants naturally encountered by r~~~~t~~ft and At~~ril~i(~~,~ representing a variety of taxonomic and morphological groups, were examined (Table 1). Fifteen species were collected from natural field populations near Woods and MPOLI~~~II.& idlrl ) were Hole. Mass. ; the remaining three (H_prtr, GI.NcI’/LII.ICI. taken from mass outdoor cultures maintained at the Environmental Systems Laboratory, Woods Hole Oc~anog~phjc InstitLltion. Only macroalgae free of attached epiphytes were used; although smalt amounts of‘epiphytic diatoms and microalgat
16
M. E. NICOTRI
may have been present, (plants
obviously
Intraspecific
effort
was made to minimize
fouled by diatoms variability
variation
due to this source
were not used).
was minimized
by using freshly collected
physiological condition and by sampling over a restricted however, due to the number of tests run, work continued
plants
in good
seasonal span (spring): from February through
July. As a result, some seasonal variation in plant quality may be present in the data. Several algal characteristics relevant to herbivore nutrition were examined. Samples were oven-dried at 50°C for 48 h to determine water content and then combusted at 450 “C for 5 h to determine ash-free dry weight. Other dried samples were subjected to analysis on a Perkin-Elmer 240 clemental analyzer to estimate percent composition of nitrogen. Caloric contents have been measured by Paine fli Vadas (1969b) and by Carefoot (1973) for west coast representatives of many of the east coast algae used in this study; these ‘literature’ values have been used here. but should be viewed cautiously in this context. In the absence of other data. these values should be adequate as first approximations. The contribution that an alga makes to the nutrition of a grazer is dependent both on the absolute content of the ‘substance’ being considered (i.e. organic matter. calories, etc.) and on the rate at which that alga is ingested. Grazing rates were obtained from a set of experiments in which isopods were given access to only one plant species at a time. Pre-weighed amounts of each alga were placed in separate containers in a water table (at 20°C) and five large isopods were added to each container; three replicates per alga N’ere run. After five days, isopods were r,:moved and the algae reweighed. Grazing rates were then calculated after correction for weight changes in ungrazed controls. An attractiveness hierarchy was constructed using a 5-l testing chamber which was divided into five interconnecting compartments. Equal weights of two species of algae were added alternately to the four corner compartments and 40 adult isopods were released into the central (empty) space. lsopods actively explored the whole chamber and moved freely from one section to another: after IL3 h, exploratory behavior markedly declined. Access between compartments was then closed and the number of isopods in each section was recorded. This procedure was repeated with a fresh batch of animals and with algae rotated between compartments (to c(\rrect for possible differences between them). The total number of individuals choosing each alga for all comparisons involving that alga was then summed and divided by the total number of isopods involved in that set of experiments to arri\,c at an attractiveness index. Thus, higher scores indicate greater attractiveness. The testing procedure was the same for A177pitl7w as the grazer. Since .4~77pithoc tends to cling to surfaces. it had difficulty moving between compartments; theret’orc. an unpartitioned testing chamber M~S used. Only 16 plant species were compared. because H~~pr7co and Dic~~~~.sipl7077 were no longer available. An experiment was devised to test the hypothesis that isopods respond to plant morphology rather than to qualities affecting food value. Plastic plants of two types
HERBIVORE
were used: one was highly branched a whorled,
monocot
two attractive
FOOD
with small leaves (rose type) and the other was
type. The attractiveness
and two unattractive
17
PREFERENCE
of these plastic plants was tested against
live species in the manner
already
described.
An edibility hierarchy was determined for Idotru but, due to time constraints. not for Ampithoc>. Grazing rates were obtained as earlier described. except that hcrc algae were offered in pair-wise combinations rather than singly. To determine a hierarchy, the mean grazing rate was calculated over all combinations involving each alga. Grazer growth rates were determined by rearing juveniles of both crustacean spcties on various kinds of algae at 20 “C. For each alga, 20 juveniles of each grazer were individually reared and changes in total body length were measured weekI\.: fresh algae. in excess of consumption needs. were supplied weekly. RESULTS ALGAL CHARACTERISTICS Table 11 details some characteristics of algae that seem relevant to questions ot preference. The percent dry matter and, better yet. percent organic matter give an
Nutritional calculations:
characteristics “(,
weight’wcet
weight;
plants:
of marine
H,O. (wet weight
of algae
‘I,, N. weight
three replicatcs
N/dry
*eight
I,, Organic 0
Data
from
Paine & Vadas (1969b)
useight;
alga: caloric
content.
‘I<, organic
matter.
calories/mg
percentage ash-l’rec
dry
dry wapht.
matter ,I
I,
Rank
3.9
IX
I.38
I0
I .x7
Y
Il.5
*
of each species were averaged.
dry weight)‘wet
0
Rank I4
Calories
Rank
2.67
Y
3.60
3
Y.3
I3
I .86
I0
.LOX
x
13.2
7
1.71
I I.5
4.51
2
20.2
I
2.03
x
16.8
4
3.67
4
-3.43
5
14.7
2.71
6
II.1
6 II
1.17
I6
16.5
5
3.09
5
3.37
7
7.x
16
1.71
I I.5
i.3Y
6
1x.x
2
7.51
7
I I.‘)
Y
I .36
I5
0.X6
IO
8.5
14
Y.5
I?
3.72
3
x.2
15
6.0
2
I7
4.lY
1’7.2
x
4.73
IX.0
3
I .hY
and Carethot
(1973).
I
4.61
I
I3
4.48
3
M. F NICOTRI
18
indication
of the amount
of solid or organic
This is highest for species like Ascoph~dlum hiclkr and Codium. calcified
material
‘per bite’ available
to grazers.
and Cltondrus and lowest for Neorr~rrrrl-
Covallina has a misleadingly
high dry matter
content
due to its
nature.
The quality of organic material will vary depending on its chemical composition. Nitrogen and caloric contents could be assumed to be important parameters that vary significantly from alga to alga. but not necessarily in similar directions. For instance. U/W and Zost~a have relatively high caloric contents. but relatively low N contents. Grazing rates for Z&IZM on individual
species
of algae are given
I I I.
3. I
1.5
15.7
5
3.X
4
3.5
0
NO ” 7 _-.
4 1
3.X
4
2 I .4
3
14.5
I .h
I0
I2
1.5
Il.5
6.7
s
4.9
2
x.1 3.3 3.8 2.9
I 4.5
0.8 0.0
3.3 2.x 2.3
4.5
3. I
7.5
0
3.X
4
0.2 0.8
17.5
0.2
15.5
14.5
I.5
I I.5
0.8
14.5
0. I
17.5
?.I
6
0.3
I4
0.x
14.5
0.X
Ii
I .8
IO
0.7
15.5
0.2
17.5
0. I
17.5
5.9
2
7.2
I.1
in Table
II
2.0
‘1
Ii.7
(1
0.X
‘1
0.4
I c:
3X.1
I
13.1
i
The amount of organic matter ingested per unit time was calculated by multiplying grazing rates by organic content. In a similar manner. caloric intakes were obtained. Again. a wide range of values is evident for both organic and caloric intakes; species with soft bodied blades like Po~plt_~x~, Ulru. and Et~t~vvtwo~ph~t have high yields and tough substantial plants like ~UCU,Sand CotwIIiw have low yields. However, it should be remembered that each alga’s contribution to herbivore nutrition will be further modified by differences in assimilation efficiency (Lowe & Lawrence, I976 : Vadas. 1977).
HERBIVORE
Table IV shows the attractiveness Attractive
FOOD PREFERENCE
hierarchies
species occur in all taxonomic
constructed
groups,
reflecting
of their diets. Morphologically robust species are preferred softer filaments and blades, which are favored by Awpitkar.
19
for I~‘otcrr and AntpitlrocJ. the generalized by /&tc~
nature
to those with
Rank
Since the algae most attractive to iclorert are large. tough plants, it could be that isopods are responding, at least proximately, to algal morph~~l~?gy rather than food value. Table V gives the results of a set of experiments testing live algae against plastic plants having morphologies hypothesized to be attractive. Isopods sometimes choose the real plant and sometimes do not discriminate between live and plastic plants. Plastic plants are significantly preferred to unattractive live species. This is evidence that attractiveness is measuring factors not related to feeding. When attractiveness is examined in relation to algal life history type (using the Kruskal-Wallis one-way analysis of variance), it is seen that i&tc’cr strongly prefers perennials over either annuals or ephemerals (Table VI). Arq~ithe, however, prefers annuals and ephemerals to perennials.
M. E. NICOTRI
20
Spearman
rank correlation
tween attractiveness
coefficients
and various
were calculated
other characteristics
to assess the relation
of the algae (Table
bc-
VII). For
The comparatlvc attractiveness of natural and artifical plants: plastic plants (rose and monocot) ~cerc tcatcd against attractive algal species (Cotliumand Frrc,rr.c)and against unattractive algae (P~~~/J//I~~u.(‘<,r(/miur~); the number of isopods on each plant is shown: 2 trials are summed: *. 7: significant at P < 0.05. Rose C~0~l/lUll
34
F1lW.S
38
Po,pll,l~ro
74 58
C’cwrn1iun1
Preference
Alga 41 40 4 IX
Monocot
x2 0.84 0.05 62.82* 21.05’
Alga
20 26 72 46
;/’
60 54 x I ‘1
20.0(1* 0.X* 51 .?(I* I I .2’”
as a function of algal life history: means for each life history type arc calculated Table IV and compared by KruskaL Wallis one-way analysis of variance. Pcrcnnials
Annuals
from
Ephemerals
Mean attractiveness
(It/orcw)
54.7
43.9
46.9
P < 0.01
12.3
43.2
39.5
P < 0 05
16.5
IO.0
15.9
I’ < O.Z!O
Mean attractiveness
(Ampithw) Mean edibility
(/rlorcw)
Spewnan
rank correlation
coefficients:
*. values
significant
at P < 0.05: numbers
I(lorcw Attractiveness Algal organic
“o N Caloric content Organic intake Caloric intake Edibility Growth
content
0.15(18) -0.48(16)* - 0.67( IO)* -().15(1X) -0.41(10) 0.31( 16) 0.03( 17)
Edibility ~0.2( 16) -0.12(16) -0.35( IO) 0.43( Ih)* 0.25( 10) 0.54(15)*
in parentheses
= :I’. _
.‘lflI/Illlllll~ Grow, th
Attracti\-encsb
0.70( 17) 0.30(15) O.I5(9) 0.61(17)* 0.Y.q’))
-0.40(16) 0.31(16) 0.4X( IO)
(irowtll ~ 0.04( 15) O.Ih(l5) ().33(c))
0.47(15)*
Idotru, organic content shows no relation to attractiveness, and (:
HERBIVORE
either organic not choosing
or caloric
intake.
to locate themselves
21
FOOD PREFERENCE
This means
that these isopods
in algae that return
and amphipods
the most nutritional
are
yield to
them.
EDIBILITY
Mean grazing rates calculated from experiments where algae were offered in pair-wise combinations (edibility. Table IV) are greater than rates observed when each species was offered individually (Table 111). Similar observations were made by Lowe (1974, cited by Lawrence, 197.5) for sea-urchin grazing. Other studies have found the converse. that algae offered singly are consumed faster than when offered in combination (Leighton. 1971 ; Vadas, 1977). Although it is uncertain why different trends have been observed, it is clear that experimental design will affect the results obtained. A variety of taxonomic and morphological types are highly edible, with both tough, robust species and soft, filamentous or bladed ones being highly consumed. A Kruskal-Wallis one-way analysis of variance (Table VI) confirms that no significant differences in edibility exist among means for perennials. annuals, or ephemerals. in contrast to the significant differences observed in attractiveness. Edibility does not correlate well with attractiveness (Table VII). This is further evidence that isopods are not attracted to algae solely by food considerations. Edibility does not correlate well with organic content, “(, N, caloric content. or caloric intake (Table VII). In agreement with these data. Paine & Vadas (1969b) and Carefoot (1973) found that preference in a variety of marine herbivores bears little relation to caloric content. Calories may not be a meaningful measure of food value since many of the carbohydrates of an alga are structural and indigestible by grazers (Lawrence, 1975). Westoby (1974) commented that palatability may or may not be related to plant nutritional value. The relation between edibility and organic indicates that animals graze faster on foods material. This makes sense evolutionarily, of those foods that produce highest yields.
intake is significant (P < 0.05) and from which they get more organic
for selection
should
favor
eating
more
GROWTH
For Iu’otea, growth varied from a low of0.3 mm/week on Zostcrcr or Ncollg~l~cllliellrr~ll~~ to 1.X mm/week on Sq~tosiplzon (Table IV). There is no correlation between growth and attractiveness, or between growth and organic content, “(, N, caloric content. or caloric intake (Table VII). However, growth does show a significant correlation with edibility and organic intake. These data again support the hypothesis that isopods are not choosing algae on the basis of food value. For Ampitlzoe, the only significant correlation is that between growth and
22
M.fl.NICOTRI
attractiveness;
this suggests
that
Ampithoe
preferences
are
more
related
to the
food value of the algae than are those of Z&~W.
DISCUSSION
Much of the literature concerning terrestrial herbivore food preference centers on the presence of a number of secondary plant compounds thought to deter grazing (Dethier. 1954; Fraenkel, 1969; Feeny. 1970; Jones, 1973; Rhoades & Cates, 1976). It is becoming clear that chemical defense is employed by a number of marine algae. although much remains to be learned in this area. Tannins occur in F~rcu.r.Srrr~~qrr.s.vum. and Ascoph~dlum (Conover & Sieburth. 1965; Sieburth. 1969). A number of halogenated compounds are widespread, especially in red algae (Fenical. 1975): some of these have been hypothesized to be anti-microbial (Hornsey & Hilde, 1974). but could play an anti-herbivore role as well. A wide variety of other toxic chemicals are known in algae and presumably function against herbivores (Ogden & Lobel. 1978). Herbivores may be differentially susceptible to such chemicals. depending on the possession of alternate metabolic pathways or detoxification capacities (Freeland & Janzen, 1974). Very little information of this nature is available for marine herbivores. 1have no data on theextent to which algal chemical defense affects isopcld or amphipod grazing. Cates & Orians (197.5) have argued that early successional (or “r-selected”) plants gain a measure of protection from herbivores byibeing unpredictable in space and time. Therefore, such plants devote less energy to anti-herbivore chemical defenses and, hence. should be preferred by generalist herbivores to later successional (“Kselected”) species. Slug grazing supports this predicted pattern. Here, although attractiveness ratings by Ampithoe are in accord with the prediction. those for Idotw follow
an opposite
successional choose algae The robust year. There
trend
(Table
VI). Edibility.
for Ihtcw.
shows
no relation
to
state. These observations also support the contention that isopods for qualities largely unrelated to feeding. algae favored by Idotcw are all perennial and available throughout the is some evidence that predictability of the resource is important In
determining preference. Paine & Vadas (I 969b) concluded that for a variety of maritre herbivores highly preferred algae tend to be those perennials (or those uithout strong seasonal components) forming a predictable, dependably available resource. Feeny (1976) has reached similar conclusions for terrestrial insects. while Otte ( 197.5) and Futuyma (1976) have used this argument to explain grasshopper and lepidopteran preferences respectively. There are several other reasons why there could be strong selection for ft/orc~/ to prefer robust algae. The morphology of these plants provides secure surfaces for small herbivores to grip. idotcu is most common in areas of modcrate to heavy wave action (Sywula, 1964; Lubchenco, pers. ohs.). There could be strong sclcctive
HERBIVORE
pressure
to choose
seaweeds
that
FOOD
PREFERENCE
provide
secure
23
clinging
sites under
surf-swept
conditions. Tough,
branched
Because isopods 1936). selection
algae
may also offer
refuge
may make up an important could be strong
from
predators,
especially
fish.
part of the diets of some fish (Larsen.
for isopods
to seek shelter in algae that offer hiding
places. Brower (1958) has proposed that some insect plant preferences may similarly be selected for by bird predation. Likewise, Anzpithoc preferences may be a corn,promise, taking into account a plant’s food value. suitability for tube-building. protection, etc. COMPARISON
OF PREFERENCES
OF THREE
MARINE
HERBIVORES
Because the attractiveness of various algal species to Liftori~cr littotw has been measured in a manner very similar to that used here (Lubchenco, 1978). some interesting
comparisons
are posible
(Table
VIII).
Preferences
of Litrorinrr
and
T.\HLI VIII Preltrcnces
(based on attractiveness)
of three herbivores: H, highly prel’erred ranking; L. low rankIng (lower
of plants tested): M. medium preference
lr?lprr/loc~ wlitltr
L H M H L M M M L H M M
(approximately
upper
I3
I ‘3 of species tated). Lif/or/f/o
lilto,.erl*
H H H L L H H H L M
H M H L
H
Ampith are similar (though not identical), while those of Idotecr are almost inverse. Why might this be? First, /dotea moves more freely than either of the other two. It can spend most of its time in algae that offer favorable habitat characteristics and still make trips to nutritious food sources; habitat and nutritional aspects of algae can be handled separately. Arnpithor, although capable of spurts of rapid
24
M. I:. NICOTRI
swimming,
stays in its tube and moves outside
slow-moving
snail.
characteristics, in arriving
Such animals
but must balance at preferences.
For
cannot
only when necessary;
habitat
and
the two sets of selective pressures
against
each other
animals.
separately
Littorinrr is a
with
these
deal
attractiveness
should correlate closely. There are hints that, for Ampithoc and Littorinn, important than dietary ones in molding preferences. calmer waters (Bousfield, 1973; Lubchenco, 1978) habitat offering support and protection from wave nerable to predators as well, for Littorina has a hard
and
edibility
food scales
habitat considerations are less These animals tend to inhabit and may have less need for a energy. They may be less vulshell and Ampithoc~ rarely leaves
its tube. Because algae may serve as habitat as well as food for many herbivores (and t’specially for small sedentary or slow-moving ones), it will be difficult to make broad generalizations about preferences. Information about the life-style of an organism will be necessary, for food preferences may be influenced to a great degree by nonnutritional factors.
ACKNOWLEDGEMENTS
This research was supported in part by the Jessie Noyes Foundation, NOAA/Sea Grant no. 04-6-158-44016, and the 1J.S. Dept. of Energy EY-76-S-02-2948AOI. I would like to thank J. Ryther, T. Losordo, and P. Clarner for use of facilities, help with construction of testing chambers, and nitrogen analyses. J. Lubchenco and B. Menge provided data. stimulating discussion, and advice. The manuscript benefited from helpful criticism from G. H. Orians.
REFERENCES
of plants
BI VAN, W. W.. K. S. BKOL\ h. JR & L. E. <;II tu ~1. lY76. Coe\olution Ilowrr BOL,~I I,
butterflies. LD.
E. L..
and herbivore\:
pa\\ion
Eoolutior~, Vol. 26. pp. 65’9 -680. I Y73. S’hu/lo~~~WO~L’I’gommaridem
Press. Ithaca. N.Y.. 312 pp. BKOW~K. L.P.. 1958. Bird predation
Awyhipodrr
and food plant
speciticlty
o/ h’cu G~,y/mtl.
(‘orllril Uni~erailq
in closely related
prncryptlc
inset-s.
Anr. ,Vo/.. Vol. 92. pp. 1X3-187. CAKI.~
WI. T. H.. 1967. Growth and nutrition of Ap/~.sio pwrc’ftrrr/ feeding on a variety of marine algae. J. ,r,ur. hid. Ass. C’.K., Vol. 47, pp. 565 58Y. C,\KI I OOI. T. H.. lY73. Feeding. food preference. and the uptake of food energy hq the aupralittoral isopod Li,yitr puNtr.sii. Mtr~. Bid.. Vol. IS. pp. 238 235
c‘x I kj,
R. G. & G. H. ORIANS.
1975. SuccesGonal
status and the palatability
herbivores. Ewlog~~. Vol. 56, pp. 410--41X pp. COI \q,h. J.. 1940. On the faunas inhabiting intertidal 129 -182. Co*\ov~ K. J. T. & J. M(‘N. animal
survival
J. L. McLachlan,
sca\%eeds. .I
of plant\
,uu/-. hrol. il.\\.
SII B~IRI H. 1965. Effect of tannins excreted In.
Vol.
24. pp.
from P/wcwp/r~~ro on planhton~c
Proc. l’th h/cvwtr// Secrwcw/ .S~,mp.. edited Pergamon Press, Oxford, pp. 2077208.
in tidepools.
L K
to gencralixd
by E. G.
\r’oung
&
HERBIVORE
D,~HL, A. L., 1964. Macroscopic
FOOD
25
PREFERENCE
I ‘X,w. Vol.
algal food of I~r/twirzrr p/o/ztr.vi.\ and I.. vrwr&r,tr.
7. pp.
1X-143. Dr I-III~K. V. Ci.. 1054. Evolution
of feeding preferences
in phytophagous
insects. Ew/rr/io,~.
Vol. X. pp.
33. 54.
I HI1 K.
DI
V. G..
1970. Chemical
E. Sondheimer DOLI\(~FK. P.M..
P.R.
terns in Colorado EIILII~\IX. Vol.
interaction
between plant and insect. In. C/wmrc~rr/ <‘(olo,~~.. edited bb
81 J. B. Simeone, Academic
Press. New York.
lupine populations.
Ocwlo,qic~ (Bwl.).
<;. F.. JK & D. N. AI \I \I>,
pp. 83~ I29
E1)~O\I
EHKI I<-H. W. L. FII~ H & D. E. BKI
1973. Alkaloid
and prcdntion
pa-
Vol. 13. pp. 19 I- 204.
197X. Coevolu~inn
in insect hcrhiborcs
and coniferr.
X wf( (‘.
199. pp. 941 945.
a study
R. & P. H. R,\\ I-X, 1964. Buttertliea and plants
EIIIILIC II.P.
in coevolution.
Ewl~lriw.
Vol.
I>:.
pp. 586 608. FI
I \Y.
I’. P.. 1970. Seasonal changes in oakleaf
tannins and nutrients
wintcrmoth caterpillars. Ecologic. Vol. 51. pp. 656 681. F-II h,. P. I’.. 1976. Plant apparency and chemical defense. t/w/ ij?.wcr\, edited by J. W. Wallace
W.. 1975.
FI h~( ,\I FKI
\hl
Vol.
I
Ci..
Halogenation
1969. Evaluation
& R. L. Mansell.
in the Rhodophyta of our thoughts
as a cause of spring fceding~ h>
In. Biotlrcw,c~o/ i~zrwoc,tro,~ /w/n~w~/ {I/“/I:,\
Plenum Publishing.
New York.
a rebieh. ./. Ph,~xo/.. Vol.
on secondary
pp. I 4(1.
I I. pp. 245 259.
plant alhstances.
&ro/w/.
c’v/?. ,-~/I,I’/..
12. pp. 473 4X6.
I-111I I .A\u, W. J. & D. H. JANT~~\. 1’974. Strategies In herbilory compounds.
bq mammals:
the role of plant wcond;~t~y
.3r,l. ,‘v’trr.. Vol. 108. pp. 269~ 789.
Fi 1~111t4. D. J.. 1976. Food
plant
specialization
and environmental
perlodicity
1n l.ep~doptcro
-I/II.
/\‘(/I.. Vol. I IO. pp. 285 292. GII HI K I L. E.. 1075. Ecological consequences of a coevolvrd
mutualiam
In. C’ww/~~/io/~ 01 unimuls Randp/n/~t.s. edited by L. E. Gilbert
between hutterllies
& P. H. Raven.
and plant\.
Uni\cr\lty
of Tear
Press. Austln. pp. 310 240. H \I
in vegetational
dicersi~y. HwoI,/~rrrw
.S\,r,,p. Rlrjl.. Vol
22.
pp. 4X 62. HI~I\II
I wtu.
J. H. & f. H. C\KE-~OOI.
seaweeds and their qgificance
1975. Seasonal changes in calorific
to home marine invertebrate
value of three Pac~l’icco;~st
hcrhiborcs.
.I ‘>\-,I. ,~wt.. Hir~l. I:‘( r~l.. Vol
IX. pp. 13% 151. HoI<\\I
\I’. I. S. & D. HII DI
I Antibiotic Hwxo.
produang
1074. The production
T. H. & G. FK \Nt KI
ccour and nonsolanaceous Hl by \hl II. c‘. B. &
C. E.
I.
1968. Selection and specificit)
plants. Afw
.
c,,rtorw/. Sot. dw..
Kt NNI I I. 1959. A
hiolopical control of Klamath J.\.Y/I N. D. H
ofnntl-microbiul
1973. Comments
IO-year
JOYI 5, D. A.. 1973. Coevolution
hcrhivoreh Acndcmic
and cyanogencs~s. In. 7‘0.ww1,~.
hcctle I’oI- x>lana-
chanec\
~~w~c~atcd with
i/&
and it\ rele\;lncc
to ~pcc~c‘~ pp. 201 212.
Pros\, Neu York.
(~c~~~/o,~I~. edited h) \:. 11. Hcy\%~>~~d.
19.36. The distribution J. M..
:lo,o
of in\crtehrates
1975. On the relationships
Bwi. .4il/l. K?l,.. Vol. 13. pp. 2 I3 286.
invertebrates
inhabiting
kelp beds. In. /‘/I[, hw/o,q~. (I/ gic//~r Xc//) h&\
.colf/lrc,r~~Ccll//w,ritr. edited by W. J. North.
I
potato 503.
Press. N. Y.. pp. 113-242.
pits and holdfasts in southern California
I. II\ HI \(
by British marlnc algae.
I?. pp. 69 X7.
of tropical
Johl \. L C‘.. 1971. Studies on selected small herbivorous
L \K\I 1. K.. p,,. I 34.
pp. 493
study of vegetational
weed. ./. /Grrr,q<,,2lgmr. Vol. on host-specificity
of the Colorado Vol. hi
richncsa. In. 7o.\-o/1ori!l,trrlt/c,c,o/o,~~,.edited by V. H. Hcqwood. Academic
compounda
marine algae. BK P/IJw/. J.. Vol. 9. pp. 353 361.
Ilcth~,i,vM~(SuppI.).
plant\
ano-
(Macrocq\ti\)
,,i
Vol. 32. pp. 343 367.
in the Dyhso Fjord.
between marine
.Ilr/c ,.,,(‘I’.\,,!
/x’c,/j_~C,II RIII/
and rw
urchin\
S//r
Vol. -II
O<~
26
M. II. NlCOTRl
: Echinoidea)
(Echinodermata Lt H( HI ~(0.
for selected marine plants. .l. ox,>. IMO~. Viol. G~ol.. Vol. I?I. pp. 22.3 3.14
J.. 1978. Plant species diversit), in a marine
vore food preference and algal competitive M.\x\..
K. H. & Bitt\.
1972. The relation
J. I;ivl/ Rev. Btl Cm..
I rv)t.
M\
I
I9
Mc N 21 (IH IO\\.
I.
I9
I. .I. S.. lY68.
Nzc,~ Vol.
13. pp. I05
between
1975. Phqtophagous
1976. Serengeti
Distribution
lobster abundance. insects as rrgulatorc
wildebeest
migratory
ecological
distribution
12.pp.
I27
of crustacean
herbivores
1976. Some aspects of herbivore-plant
D.. 1975. Plant preference and plant succession. O~~lo~g;r/ R. T. & R. L. V,\IIAS.
1969a. The effects of grazing
0..
on the microflora
34. pp. I:~~I/~I~~I.
seaweed population\.
4q~c/-
food preference. 196’). Bcnthic
on Caribbean
reel\
and \capraa\
(Ed.).
Vol. 18. pp. I2Y
144.
by sea urchms. S~~o,?,ql/oc,c,,rr~ot~c\spp
w
Occw/ro~q~.. Vol. 14. pp 7 I O&719.
Limd.
P.IINF. R. T. & R. L. V~D,%S. 1969b. Caloriflc \hho.
Vol.
fishes and urchins in coral reef commun-
I I1
RI\
.I. UU,UI. l<~~~l/
hiol. ily.5. ( .k..
herbivores
relatlonships
fi/fl,. Ri0/. F&h.. Vol. 3. pp. 4Y 63.
benthic algal populations.
of Itk~rc,~/ (Isopoda).
on cultured
tie\
to invertebrate
flolu by grar~~tz.
136.
beds. Ayf,U//<~ Ho/.. Vol. 7. pp. IO.3 Ilh. O(,r,t v. J. c‘. & P.S. Lonr I 1 197X. The role of herbivorous
P,IIN~.
of energy
of /&~<,rr. ./. ~x,r.
effects of four marine IntertIdal
Vol. 58. pp. 1020-1032. NIC OI 111. M. E.. lY77b. The impact
0
production.
plants. (‘o~rr. ,?u,,‘. .S(I. ( U/I‘. /;,.\
of British spccia
lY55b. The diet and feeding mechanism
O(;DI L. J. C..
and kelp htxis.
of forest primary
: Facilitation
of the epihiota of macroepibenthic
347 355. ‘UICOI KI, M. E.. IY77a. Grazing
U///U,~?. Vol.
sea urchin\,
144.
I OK.E.. lY55a. The Vol. 34. pp. 255 260. IOI<. t..
of herhi-
pp. 92-Y4.
N \\ NI\
importance
pp. 92-94.
S. J..
sc;c/rcx,. Vol
community:
Vol. 29. pp. 603-605.
W. J. & N. D. Aor11.
.S~~i(‘/U.(‘.Vol.
intertidal
abilities. Am. ,‘Vtrr.. Vol. I 12. pp. 2%39.
values of benthic marine algae and their postulated
relation
:Mu~. Bbjl.. Vol. 4. pp. 7Y 86.
algae ah I’ood for some In\ertcbrxrcs
m the inner
part of the Ball c.
I-i,l/frob?S,c,tr. Vol. 7. pp. 2oi- 205.
R>
I HI IN.J. H.. J.C. <;ol IIRIZU, I I,\M\ & 8. E. L.\I~INII.
WII
culture \lstems.
Ci E. <;[I TORI). lY75.
Physical
ily1itrcr1/111~~.Vol. 5. pp. I63
SII HIIKI II. J. Mc N..
.I E.
Hr (8,
models
I \I,\.
A.S.
on integrated
M:I\(,. haste
J.P.
c‘i \,<\I
recycllns
II. I.
marlnc
Il.
polb-
177.
1069. Studies on algal substances 111the ~a.
III.
The production
of c\traccIIuI.Ir
orsr;tntc matter bj Ilttoral marine algae. ./. <‘x-p ,1x/r. H/o/. I!?~~/.. Vol. 3. pp. 311 iO9 Shl I( 11. A. F.. 1926. On the habits and ecology of the tube-building amphipod A/~/>//hoc, ~-f,hr,c~rr~~ Mollt~Lgue.
EuJ/o,ql.
Vol.
7. pp. 4x l--502.
FACTORS
INVOLVED
IN HERBIVORE
FOOD
PREFERENCE’
Abstract: Herbivore food preference can be measured etther in terms of attractivcnesb or of edibllit) : these quantitlcs are not necessarily correlated. The isopod I~/o/ctr h~//ic~o (Pallas) is attracted to large. tough. branched algae (perennials) while the amphipod .Anlpirhoc~ ~rliclrr (Smith) is attracted to softer. filamentous or bladed algae (ephemerals). Attractivenchs for Anz~~irhoc~is related to the nutritive value ofthe algae; this is not so for I~lot~. which responds more to algal morphology and availability. /t/~rctr‘\ mobility. possible susceptibility to fish predation. and prcfcrcnce for moderate v,a\c‘ eupo\ures mnq select for a primary response to alpac as habitat rather than as food source.
Herbivore food preferences are of considerable theoretical and practical interest to ecologists. Preference determines the quantity and quality of food ingested by a grazer and hence affects its physiological condition and fitness (Hsiao & Fraenkel. 1968). Herbivore preference also interacts with plant competitive abilities, life hiatories. and physical tolerances to determine the impact of a grazer on the plant community (Lubchenco, 1978). Frequently, herbivore effects on plant distributions. biomass, and diversity are dramatic (Huffaker & Kennett, 1959; Harper, 1969; Paine & Vadas. 1969a; Mann & Breen. 1972; Janzen. 1973; Mattson & Addy, 1975; McNaughton, 1976; Snyder & Janke, 1976). Furthermore. the relationship between plants and herbivores is not static; each may effect evolutionary change in the other (Ehrlich & Raven, 1964; Dethier. 1970; Dolinger c’t 01.. 1973: Freeland & Janzer~. 1974; Gilbert. 1975; Benson CI [I/.. 1976; Edmunds & Alstad. 1978). Two distinct components of food preference are commonly recognized: one relnting to the selection of a potential prey item (attractiveness). and the other relating to the rate at which that prey is ingested (edibility). Attractiveness is measured by methods that permit herbivores to choose betbeen several possible foods. This may involve chemoreception over some distance (Vadas. 1977) or it may involve direct chemical and tactile sampling of plants (Himmelman & Carcfoot, 1975: Lawrence. 1975: Lubchenco. 1978). Methods dealing with edibility assume that. under equivalent hunger conditions, herbivores consume preferred items faster (Leighton & Boolootian. 1963: Carefoot, 1967); edibility will retlect not only the speed with which a given item satisfies the physiological needs of a herbivore, but also the ease
M. E. NIC’OTRI
14
with which that item is handled edibility
have sometimes
are distinct
and measure
and ingested.
In the literature,
been used interchangeably; different
aspects of preference
Preference may be influenced by factors not relating ties of the plant. For instance, small aquatic herbivores
however,
attracti~~encss
and
it is clear that they
(Lawrence,
1975).
directly to nutritional qualithat live nestled among algnl
fronds may utilizean alga as habitat as well as food source. The amount of protection offered from predators or the amount of shelter from wave action are irnport~~t~t habitat characteristics (Colman, 1940; Wieser. 1952; Nagle, 1968) and might influence herbivore choice as much as the food value of the plant. The predictability of plant presence in space and time is also important and, in evolutionary terms, may affect herbivore preferences (Paine & Vadas, lY6Ya: Feeny, 1976). Preference has been studied in a number of marine herbivores. Investigators generally have concentrated on sea urchins (extensively reviewed by Lawrence, 1975; Vadas, 1977). molluscs (Leighton & Boolootian, 1963: Dahl, 1964; Leighton. 1960: Carefoot, 1967; Himmelman & Carefoot, 1975; Nicotri. lY77a; Lubchenco. lY78). and fish (Tsuda & Bryan, 1973; Vine, 1974; Ogden, lY76: Ogden & Lobcl. lY78). There is some illformat~on available about the diets of noi~plankt~~nic ~lerbivor~~~ls crustaceans (Ravanko, 1969; Jones, 1971; Carefoot, 1973). but, in general, pref’crences of this grou’p are poorly known. This is unfortunate since such crustaceans are common and often quite abundant. This study was designed to examine the food preferences of two of these crustaceans, the isopod Ihtcm hrrlticn (Pallas) and the amphipod ,~~~irlz~~~~wlidu (Smith). After factors that influence both components of preference have been investigated. results of this study are compared with preferences of the periwinkle Littorirra littolwr. an extremely common and abundant marine gastropod studied by Lubchenco (1978). Since the distribution of Littori/rt/ broadly overlaps that of I&~M and Anpith and all three grazers could potentially be using the same plants, it is of interest to compare the similarity of t’ood preferences. I&~LJLIholticu is an active isopod found among seaweeds in intertidal and very shallow subtidal zones throughout temperate latitudes (Naylor. 1Y55a). It is herbivorous (Naylor, 1955b; Ruvanko. 1969) and is an extremely abundant potential pest in a polyspecies aquaculture system at Woods Hole Oceanographic Institution. Cape Cod. ~ass~~chusetts (Ryther of (I/.. 1975: Nicotri, IY77b). it is also an opportunistic scavenger (Sywula, 1964) and is cannabalistic at high densities. It grolvs on available food. and may reach sizes of 3 cm fast, up to 2 mm/week, depending (Nicotri, 1977b). A7~7pir/7~w IU/~&I is a sedentary tube-dwelling amphipod, rarely leaving its tube except under duress (Skutch, 1926). It may reach very high local densities (Bousficld, 1973) and often does so in the aquaculture system at Woods Hole (Nicotri. 1977b). Since movement is limited and the alga chosen becomes both habitat and rood source, initial settlement is quite important. However, under adverse conditions. individuals can and do move and are capable of swimming rapidly for short periods.
HERBIVORE
Growth maximal
averages
about
I mm/week
body length is about
under
conditions
I .8 cm (Nicotri,
MATERIALS
15
FOOD PREFERENCE
AND
of optimal
food a~~il~~bilit~ :
1977b).
METHODS
Eighteen species of marine plants naturally encountered by r~~~~t~~ft and At~~ril~i(~~,~ representing a variety of taxonomic and morphological groups, were examined (Table 1). Fifteen species were collected from natural field populations near Woods and MPOLI~~~II.& idlrl ) were Hole. Mass. ; the remaining three (H_prtr, GI.NcI’/LII.ICI. taken from mass outdoor cultures maintained at the Environmental Systems Laboratory, Woods Hole Oc~anog~phjc InstitLltion. Only macroalgae free of attached epiphytes were used; although smalt amounts of‘epiphytic diatoms and microalgat
16
M. E. NICOTRI
may have been present, (plants
obviously
Intraspecific
effort
was made to minimize
fouled by diatoms variability
variation
due to this source
were not used).
was minimized
by using freshly collected
physiological condition and by sampling over a restricted however, due to the number of tests run, work continued
plants
in good
seasonal span (spring): from February through
July. As a result, some seasonal variation in plant quality may be present in the data. Several algal characteristics relevant to herbivore nutrition were examined. Samples were oven-dried at 50°C for 48 h to determine water content and then combusted at 450 “C for 5 h to determine ash-free dry weight. Other dried samples were subjected to analysis on a Perkin-Elmer 240 clemental analyzer to estimate percent composition of nitrogen. Caloric contents have been measured by Paine fli Vadas (1969b) and by Carefoot (1973) for west coast representatives of many of the east coast algae used in this study; these ‘literature’ values have been used here. but should be viewed cautiously in this context. In the absence of other data. these values should be adequate as first approximations. The contribution that an alga makes to the nutrition of a grazer is dependent both on the absolute content of the ‘substance’ being considered (i.e. organic matter. calories, etc.) and on the rate at which that alga is ingested. Grazing rates were obtained from a set of experiments in which isopods were given access to only one plant species at a time. Pre-weighed amounts of each alga were placed in separate containers in a water table (at 20°C) and five large isopods were added to each container; three replicates per alga N’ere run. After five days, isopods were r,:moved and the algae reweighed. Grazing rates were then calculated after correction for weight changes in ungrazed controls. An attractiveness hierarchy was constructed using a 5-l testing chamber which was divided into five interconnecting compartments. Equal weights of two species of algae were added alternately to the four corner compartments and 40 adult isopods were released into the central (empty) space. lsopods actively explored the whole chamber and moved freely from one section to another: after IL3 h, exploratory behavior markedly declined. Access between compartments was then closed and the number of isopods in each section was recorded. This procedure was repeated with a fresh batch of animals and with algae rotated between compartments (to c(\rrect for possible differences between them). The total number of individuals choosing each alga for all comparisons involving that alga was then summed and divided by the total number of isopods involved in that set of experiments to arri\,c at an attractiveness index. Thus, higher scores indicate greater attractiveness. The testing procedure was the same for A177pitl7w as the grazer. Since .4~77pithoc tends to cling to surfaces. it had difficulty moving between compartments; theret’orc. an unpartitioned testing chamber M~S used. Only 16 plant species were compared. because H~~pr7co and Dic~~~~.sipl7077 were no longer available. An experiment was devised to test the hypothesis that isopods respond to plant morphology rather than to qualities affecting food value. Plastic plants of two types
HERBIVORE
were used: one was highly branched a whorled,
monocot
two attractive
FOOD
with small leaves (rose type) and the other was
type. The attractiveness
and two unattractive
17
PREFERENCE
of these plastic plants was tested against
live species in the manner
already
described.
An edibility hierarchy was determined for Idotru but, due to time constraints. not for Ampithoc>. Grazing rates were obtained as earlier described. except that hcrc algae were offered in pair-wise combinations rather than singly. To determine a hierarchy, the mean grazing rate was calculated over all combinations involving each alga. Grazer growth rates were determined by rearing juveniles of both crustacean spcties on various kinds of algae at 20 “C. For each alga, 20 juveniles of each grazer were individually reared and changes in total body length were measured weekI\.: fresh algae. in excess of consumption needs. were supplied weekly. RESULTS ALGAL CHARACTERISTICS Table 11 details some characteristics of algae that seem relevant to questions ot preference. The percent dry matter and, better yet. percent organic matter give an
Nutritional calculations:
characteristics “(,
weight’wcet
weight;
plants:
of marine
H,O. (wet weight
of algae
‘I,, N. weight
three replicatcs
N/dry
*eight
I,, Organic 0
Data
from
Paine & Vadas (1969b)
useight;
alga: caloric
content.
‘I<, organic
matter.
calories/mg
percentage ash-l’rec
dry
dry wapht.
matter ,I
I,
Rank
3.9
IX
I.38
I0
I .x7
Y
Il.5
*
of each species were averaged.
dry weight)‘wet
0
Rank I4
Calories
Rank
2.67
Y
3.60
3
Y.3
I3
I .86
I0
.LOX
x
13.2
7
1.71
I I.5
4.51
2
20.2
I
2.03
x
16.8
4
3.67
4
-3.43
5
14.7
2.71
6
II.1
6 II
1.17
I6
16.5
5
3.09
5
3.37
7
7.x
16
1.71
I I.5
i.3Y
6
1x.x
2
7.51
7
I I.‘)
Y
I .36
I5
0.X6
IO
8.5
14
Y.5
I?
3.72
3
x.2
15
6.0
2
I7
4.lY
1’7.2
x
4.73
IX.0
3
I .hY
and Carethot
(1973).
I
4.61
I
I3
4.48
3
M. F NICOTRI
18
indication
of the amount
of solid or organic
This is highest for species like Ascoph~dlum hiclkr and Codium. calcified
material
‘per bite’ available
to grazers.
and Cltondrus and lowest for Neorr~rrrrl-
Covallina has a misleadingly
high dry matter
content
due to its
nature.
The quality of organic material will vary depending on its chemical composition. Nitrogen and caloric contents could be assumed to be important parameters that vary significantly from alga to alga. but not necessarily in similar directions. For instance. U/W and Zost~a have relatively high caloric contents. but relatively low N contents. Grazing rates for Z&IZM on individual
species
of algae are given
I I I.
3. I
1.5
15.7
5
3.X
4
3.5
0
NO ” 7 _-.
4 1
3.X
4
2 I .4
3
14.5
I .h
I0
I2
1.5
Il.5
6.7
s
4.9
2
x.1 3.3 3.8 2.9
I 4.5
0.8 0.0
3.3 2.x 2.3
4.5
3. I
7.5
0
3.X
4
0.2 0.8
17.5
0.2
15.5
14.5
I.5
I I.5
0.8
14.5
0. I
17.5
?.I
6
0.3
I4
0.x
14.5
0.X
Ii
I .8
IO
0.7
15.5
0.2
17.5
0. I
17.5
5.9
2
7.2
I.1
in Table
II
2.0
‘1
Ii.7
(1
0.X
‘1
0.4
I c:
3X.1
I
13.1
i
The amount of organic matter ingested per unit time was calculated by multiplying grazing rates by organic content. In a similar manner. caloric intakes were obtained. Again. a wide range of values is evident for both organic and caloric intakes; species with soft bodied blades like Po~plt_~x~, Ulru. and Et~t~vvtwo~ph~t have high yields and tough substantial plants like ~UCU,Sand CotwIIiw have low yields. However, it should be remembered that each alga’s contribution to herbivore nutrition will be further modified by differences in assimilation efficiency (Lowe & Lawrence, I976 : Vadas. 1977).
HERBIVORE
Table IV shows the attractiveness Attractive
FOOD PREFERENCE
hierarchies
species occur in all taxonomic
constructed
groups,
reflecting
of their diets. Morphologically robust species are preferred softer filaments and blades, which are favored by Awpitkar.
19
for I~‘otcrr and AntpitlrocJ. the generalized by /&tc~
nature
to those with
Rank
Since the algae most attractive to iclorert are large. tough plants, it could be that isopods are responding, at least proximately, to algal morph~~l~?gy rather than food value. Table V gives the results of a set of experiments testing live algae against plastic plants having morphologies hypothesized to be attractive. Isopods sometimes choose the real plant and sometimes do not discriminate between live and plastic plants. Plastic plants are significantly preferred to unattractive live species. This is evidence that attractiveness is measuring factors not related to feeding. When attractiveness is examined in relation to algal life history type (using the Kruskal-Wallis one-way analysis of variance), it is seen that i&tc’cr strongly prefers perennials over either annuals or ephemerals (Table VI). Arq~ithe, however, prefers annuals and ephemerals to perennials.
M. E. NICOTRI
20
Spearman
rank correlation
tween attractiveness
coefficients
and various
were calculated
other characteristics
to assess the relation
of the algae (Table
bc-
VII). For
The comparatlvc attractiveness of natural and artifical plants: plastic plants (rose and monocot) ~cerc tcatcd against attractive algal species (Cotliumand Frrc,rr.c)and against unattractive algae (P~~~/J//I~~u.(‘<,r(/miur~); the number of isopods on each plant is shown: 2 trials are summed: *. 7: significant at P < 0.05. Rose C~0~l/lUll
34
F1lW.S
38
Po,pll,l~ro
74 58
C’cwrn1iun1
Preference
Alga 41 40 4 IX
Monocot
x2 0.84 0.05 62.82* 21.05’
Alga
20 26 72 46
;/’
60 54 x I ‘1
20.0(1* 0.X* 51 .?(I* I I .2’”
as a function of algal life history: means for each life history type arc calculated Table IV and compared by KruskaL Wallis one-way analysis of variance. Pcrcnnials
Annuals
from
Ephemerals
Mean attractiveness
(It/orcw)
54.7
43.9
46.9
P < 0.01
12.3
43.2
39.5
P < 0 05
16.5
IO.0
15.9
I’ < O.Z!O
Mean attractiveness
(Ampithw) Mean edibility
(/rlorcw)
Spewnan
rank correlation
coefficients:
*. values
significant
at P < 0.05: numbers
I(lorcw Attractiveness Algal organic
“o N Caloric content Organic intake Caloric intake Edibility Growth
content
0.15(18) -0.48(16)* - 0.67( IO)* -().15(1X) -0.41(10) 0.31( 16) 0.03( 17)
Edibility ~0.2( 16) -0.12(16) -0.35( IO) 0.43( Ih)* 0.25( 10) 0.54(15)*
in parentheses
= :I’. _
.‘lflI/Illlllll~ Grow, th
Attracti\-encsb
0.70( 17) 0.30(15) O.I5(9) 0.61(17)* 0.Y.q’))
-0.40(16) 0.31(16) 0.4X( IO)
(irowtll ~ 0.04( 15) O.Ih(l5) ().33(c))
0.47(15)*
Idotru, organic content shows no relation to attractiveness, and (:
HERBIVORE
either organic not choosing
or caloric
intake.
to locate themselves
21
FOOD PREFERENCE
This means
that these isopods
in algae that return
and amphipods
the most nutritional
are
yield to
them.
EDIBILITY
Mean grazing rates calculated from experiments where algae were offered in pair-wise combinations (edibility. Table IV) are greater than rates observed when each species was offered individually (Table 111). Similar observations were made by Lowe (1974, cited by Lawrence, 197.5) for sea-urchin grazing. Other studies have found the converse. that algae offered singly are consumed faster than when offered in combination (Leighton. 1971 ; Vadas, 1977). Although it is uncertain why different trends have been observed, it is clear that experimental design will affect the results obtained. A variety of taxonomic and morphological types are highly edible, with both tough, robust species and soft, filamentous or bladed ones being highly consumed. A Kruskal-Wallis one-way analysis of variance (Table VI) confirms that no significant differences in edibility exist among means for perennials. annuals, or ephemerals. in contrast to the significant differences observed in attractiveness. Edibility does not correlate well with attractiveness (Table VII). This is further evidence that isopods are not attracted to algae solely by food considerations. Edibility does not correlate well with organic content, “(, N, caloric content. or caloric intake (Table VII). In agreement with these data. Paine & Vadas (1969b) and Carefoot (1973) found that preference in a variety of marine herbivores bears little relation to caloric content. Calories may not be a meaningful measure of food value since many of the carbohydrates of an alga are structural and indigestible by grazers (Lawrence, 1975). Westoby (1974) commented that palatability may or may not be related to plant nutritional value. The relation between edibility and organic indicates that animals graze faster on foods material. This makes sense evolutionarily, of those foods that produce highest yields.
intake is significant (P < 0.05) and from which they get more organic
for selection
should
favor
eating
more
GROWTH
For Iu’otea, growth varied from a low of0.3 mm/week on Zostcrcr or Ncollg~l~cllliellrr~ll~~ to 1.X mm/week on Sq~tosiplzon (Table IV). There is no correlation between growth and attractiveness, or between growth and organic content, “(, N, caloric content. or caloric intake (Table VII). However, growth does show a significant correlation with edibility and organic intake. These data again support the hypothesis that isopods are not choosing algae on the basis of food value. For Ampitlzoe, the only significant correlation is that between growth and
22
M.fl.NICOTRI
attractiveness;
this suggests
that
Ampithoe
preferences
are
more
related
to the
food value of the algae than are those of Z&~W.
DISCUSSION
Much of the literature concerning terrestrial herbivore food preference centers on the presence of a number of secondary plant compounds thought to deter grazing (Dethier. 1954; Fraenkel, 1969; Feeny. 1970; Jones, 1973; Rhoades & Cates, 1976). It is becoming clear that chemical defense is employed by a number of marine algae. although much remains to be learned in this area. Tannins occur in F~rcu.r.Srrr~~qrr.s.vum. and Ascoph~dlum (Conover & Sieburth. 1965; Sieburth. 1969). A number of halogenated compounds are widespread, especially in red algae (Fenical. 1975): some of these have been hypothesized to be anti-microbial (Hornsey & Hilde, 1974). but could play an anti-herbivore role as well. A wide variety of other toxic chemicals are known in algae and presumably function against herbivores (Ogden & Lobel. 1978). Herbivores may be differentially susceptible to such chemicals. depending on the possession of alternate metabolic pathways or detoxification capacities (Freeland & Janzen, 1974). Very little information of this nature is available for marine herbivores. 1have no data on theextent to which algal chemical defense affects isopcld or amphipod grazing. Cates & Orians (197.5) have argued that early successional (or “r-selected”) plants gain a measure of protection from herbivores byibeing unpredictable in space and time. Therefore, such plants devote less energy to anti-herbivore chemical defenses and, hence. should be preferred by generalist herbivores to later successional (“Kselected”) species. Slug grazing supports this predicted pattern. Here, although attractiveness ratings by Ampithoe are in accord with the prediction. those for Idotw follow
an opposite
successional choose algae The robust year. There
trend
(Table
VI). Edibility.
for Ihtcw.
shows
no relation
to
state. These observations also support the contention that isopods for qualities largely unrelated to feeding. algae favored by Idotcw are all perennial and available throughout the is some evidence that predictability of the resource is important In
determining preference. Paine & Vadas (I 969b) concluded that for a variety of maritre herbivores highly preferred algae tend to be those perennials (or those uithout strong seasonal components) forming a predictable, dependably available resource. Feeny (1976) has reached similar conclusions for terrestrial insects. while Otte ( 197.5) and Futuyma (1976) have used this argument to explain grasshopper and lepidopteran preferences respectively. There are several other reasons why there could be strong selection for ft/orc~/ to prefer robust algae. The morphology of these plants provides secure surfaces for small herbivores to grip. idotcu is most common in areas of modcrate to heavy wave action (Sywula, 1964; Lubchenco, pers. ohs.). There could be strong sclcctive
HERBIVORE
pressure
to choose
seaweeds
that
FOOD
PREFERENCE
provide
secure
23
clinging
sites under
surf-swept
conditions. Tough,
branched
Because isopods 1936). selection
algae
may also offer
refuge
may make up an important could be strong
from
predators,
especially
fish.
part of the diets of some fish (Larsen.
for isopods
to seek shelter in algae that offer hiding
places. Brower (1958) has proposed that some insect plant preferences may similarly be selected for by bird predation. Likewise, Anzpithoc preferences may be a corn,promise, taking into account a plant’s food value. suitability for tube-building. protection, etc. COMPARISON
OF PREFERENCES
OF THREE
MARINE
HERBIVORES
Because the attractiveness of various algal species to Liftori~cr littotw has been measured in a manner very similar to that used here (Lubchenco, 1978). some interesting
comparisons
are posible
(Table
VIII).
Preferences
of Litrorinrr
and
T.\HLI VIII Preltrcnces
(based on attractiveness)
of three herbivores: H, highly prel’erred ranking; L. low rankIng (lower
of plants tested): M. medium preference
lr?lprr/loc~ wlitltr
L H M H L M M M L H M M
(approximately
upper
I3
I ‘3 of species tated). Lif/or/f/o
lilto,.erl*
H H H L L H H H L M
H M H L
H
Ampith are similar (though not identical), while those of Idotecr are almost inverse. Why might this be? First, /dotea moves more freely than either of the other two. It can spend most of its time in algae that offer favorable habitat characteristics and still make trips to nutritious food sources; habitat and nutritional aspects of algae can be handled separately. Arnpithor, although capable of spurts of rapid
24
M. I:. NICOTRI
swimming,
stays in its tube and moves outside
slow-moving
snail.
characteristics, in arriving
Such animals
but must balance at preferences.
For
cannot
only when necessary;
habitat
and
the two sets of selective pressures
against
each other
animals.
separately
Littorinrr is a
with
these
deal
attractiveness
should correlate closely. There are hints that, for Ampithoc and Littorinn, important than dietary ones in molding preferences. calmer waters (Bousfield, 1973; Lubchenco, 1978) habitat offering support and protection from wave nerable to predators as well, for Littorina has a hard
and
edibility
food scales
habitat considerations are less These animals tend to inhabit and may have less need for a energy. They may be less vulshell and Ampithoc~ rarely leaves
its tube. Because algae may serve as habitat as well as food for many herbivores (and t’specially for small sedentary or slow-moving ones), it will be difficult to make broad generalizations about preferences. Information about the life-style of an organism will be necessary, for food preferences may be influenced to a great degree by nonnutritional factors.
ACKNOWLEDGEMENTS
This research was supported in part by the Jessie Noyes Foundation, NOAA/Sea Grant no. 04-6-158-44016, and the 1J.S. Dept. of Energy EY-76-S-02-2948AOI. I would like to thank J. Ryther, T. Losordo, and P. Clarner for use of facilities, help with construction of testing chambers, and nitrogen analyses. J. Lubchenco and B. Menge provided data. stimulating discussion, and advice. The manuscript benefited from helpful criticism from G. H. Orians.
REFERENCES
of plants
BI VAN, W. W.. K. S. BKOL\ h. JR & L. E. <;II tu ~1. lY76. Coe\olution Ilowrr BOL,~I I,
butterflies. LD.
E. L..
and herbivore\:
pa\\ion
Eoolutior~, Vol. 26. pp. 65’9 -680. I Y73. S’hu/lo~~~WO~L’I’gommaridem
Press. Ithaca. N.Y.. 312 pp. BKOW~K. L.P.. 1958. Bird predation
Awyhipodrr
and food plant
speciticlty
o/ h’cu G~,y/mtl.
(‘orllril Uni~erailq
in closely related
prncryptlc
inset-s.
Anr. ,Vo/.. Vol. 92. pp. 1X3-187. CAKI.~
WI. T. H.. 1967. Growth and nutrition of Ap/~.sio pwrc’ftrrr/ feeding on a variety of marine algae. J. ,r,ur. hid. Ass. C’.K., Vol. 47, pp. 565 58Y. C,\KI I OOI. T. H.. lY73. Feeding. food preference. and the uptake of food energy hq the aupralittoral isopod Li,yitr puNtr.sii. Mtr~. Bid.. Vol. IS. pp. 238 235
c‘x I kj,
R. G. & G. H. ORIANS.
1975. SuccesGonal
status and the palatability
herbivores. Ewlog~~. Vol. 56, pp. 410--41X pp. COI \q,h. J.. 1940. On the faunas inhabiting intertidal 129 -182. Co*\ov~ K. J. T. & J. M(‘N. animal
survival
J. L. McLachlan,
sca\%eeds. .I
of plant\
,uu/-. hrol. il.\\.
SII B~IRI H. 1965. Effect of tannins excreted In.
Vol.
24. pp.
from P/wcwp/r~~ro on planhton~c
Proc. l’th h/cvwtr// Secrwcw/ .S~,mp.. edited Pergamon Press, Oxford, pp. 2077208.
in tidepools.
L K
to gencralixd
by E. G.
\r’oung
&
HERBIVORE
D,~HL, A. L., 1964. Macroscopic
FOOD
25
PREFERENCE
I ‘X,w. Vol.
algal food of I~r/twirzrr p/o/ztr.vi.\ and I.. vrwr&r,tr.
7. pp.
1X-143. Dr I-III~K. V. Ci.. 1054. Evolution
of feeding preferences
in phytophagous
insects. Ew/rr/io,~.
Vol. X. pp.
33. 54.
I HI1 K.
DI
V. G..
1970. Chemical
E. Sondheimer DOLI\(~FK. P.M..
P.R.
terns in Colorado EIILII~\IX. Vol.
interaction
between plant and insect. In. C/wmrc~rr/ <‘(olo,~~.. edited bb
81 J. B. Simeone, Academic
Press. New York.
lupine populations.
Ocwlo,qic~ (Bwl.).
<;. F.. JK & D. N. AI \I \I>,
pp. 83~ I29
E1)~O\I
EHKI I<-H. W. L. FII~ H & D. E. BKI
1973. Alkaloid
and prcdntion
pa-
Vol. 13. pp. 19 I- 204.
197X. Coevolu~inn
in insect hcrhiborcs
and coniferr.
X wf( (‘.
199. pp. 941 945.
a study
R. & P. H. R,\\ I-X, 1964. Buttertliea and plants
EIIIILIC II.P.
in coevolution.
Ewl~lriw.
Vol.
I>:.
pp. 586 608. FI
I \Y.
I’. P.. 1970. Seasonal changes in oakleaf
tannins and nutrients
wintcrmoth caterpillars. Ecologic. Vol. 51. pp. 656 681. F-II h,. P. I’.. 1976. Plant apparency and chemical defense. t/w/ ij?.wcr\, edited by J. W. Wallace
W.. 1975.
FI h~( ,\I FKI
\hl
Vol.
I
Ci..
Halogenation
1969. Evaluation
& R. L. Mansell.
in the Rhodophyta of our thoughts
as a cause of spring fceding~ h>
In. Biotlrcw,c~o/ i~zrwoc,tro,~ /w/n~w~/ {I/“/I:,\
Plenum Publishing.
New York.
a rebieh. ./. Ph,~xo/.. Vol.
on secondary
pp. I 4(1.
I I. pp. 245 259.
plant alhstances.
&ro/w/.
c’v/?. ,-~/I,I’/..
12. pp. 473 4X6.
I-111I I .A\u, W. J. & D. H. JANT~~\. 1’974. Strategies In herbilory compounds.
bq mammals:
the role of plant wcond;~t~y
.3r,l. ,‘v’trr.. Vol. 108. pp. 269~ 789.
Fi 1~111t4. D. J.. 1976. Food
plant
specialization
and environmental
perlodicity
1n l.ep~doptcro
-I/II.
/\‘(/I.. Vol. I IO. pp. 285 292. GII HI K I L. E.. 1075. Ecological consequences of a coevolvrd
mutualiam
In. C’ww/~~/io/~ 01 unimuls Randp/n/~t.s. edited by L. E. Gilbert
between hutterllies
& P. H. Raven.
and plant\.
Uni\cr\lty
of Tear
Press. Austln. pp. 310 240. H \I
in vegetational
dicersi~y. HwoI,/~rrrw
.S\,r,,p. Rlrjl.. Vol
22.
pp. 4X 62. HI~I\II
I wtu.
J. H. & f. H. C\KE-~OOI.
seaweeds and their qgificance
1975. Seasonal changes in calorific
to home marine invertebrate
value of three Pac~l’icco;~st
hcrhiborcs.
.I ‘>\-,I. ,~wt.. Hir~l. I:‘( r~l.. Vol
IX. pp. 13% 151. HoI<\\I
\I’. I. S. & D. HII DI
I Antibiotic Hwxo.
produang
1074. The production
T. H. & G. FK \Nt KI
ccour and nonsolanaceous Hl by \hl II. c‘. B. &
C. E.
I.
1968. Selection and specificit)
plants. Afw
.
c,,rtorw/. Sot. dw..
Kt NNI I I. 1959. A
hiolopical control of Klamath J.\.Y/I N. D. H
ofnntl-microbiul
1973. Comments
IO-year
JOYI 5, D. A.. 1973. Coevolution
hcrhivoreh Acndcmic
and cyanogencs~s. In. 7‘0.ww1,~.
hcctle I’oI- x>lana-
chanec\
~~w~c~atcd with
i/&
and it\ rele\;lncc
to ~pcc~c‘~ pp. 201 212.
Pros\, Neu York.
(~c~~~/o,~I~. edited h) \:. 11. Hcy\%~>~~d.
19.36. The distribution J. M..
:lo,o
of in\crtehrates
1975. On the relationships
Bwi. .4il/l. K?l,.. Vol. 13. pp. 2 I3 286.
invertebrates
inhabiting
kelp beds. In. /‘/I[, hw/o,q~. (I/ gic//~r Xc//) h&\
.colf/lrc,r~~Ccll//w,ritr. edited by W. J. North.
I
potato 503.
Press. N. Y.. pp. 113-242.
pits and holdfasts in southern California
I. II\ HI \(
by British marlnc algae.
I?. pp. 69 X7.
of tropical
Johl \. L C‘.. 1971. Studies on selected small herbivorous
L \K\I 1. K.. p,,. I 34.
pp. 493
study of vegetational
weed. ./. /Grrr,q<,,2lgmr. Vol. on host-specificity
of the Colorado Vol. hi
richncsa. In. 7o.\-o/1ori!l,trrlt/c,c,o/o,~~,.edited by V. H. Hcqwood. Academic
compounda
marine algae. BK P/IJw/. J.. Vol. 9. pp. 353 361.
Ilcth~,i,vM~(SuppI.).
plant\
ano-
(Macrocq\ti\)
,,i
Vol. 32. pp. 343 367.
in the Dyhso Fjord.
between marine
.Ilr/c ,.,,(‘I’.\,,!
/x’c,/j_~C,II RIII/
and rw
urchin\
S//r
Vol. -II
O<~
26
M. II. NlCOTRl
: Echinoidea)
(Echinodermata Lt H( HI ~(0.
for selected marine plants. .l. ox,>. IMO~. Viol. G~ol.. Vol. I?I. pp. 22.3 3.14
J.. 1978. Plant species diversit), in a marine
vore food preference and algal competitive M.\x\..
K. H. & Bitt\.
1972. The relation
J. I;ivl/ Rev. Btl Cm..
I rv)t.
M\
I
I9
Mc N 21 (IH IO\\.
I.
I9
I. .I. S.. lY68.
Nzc,~ Vol.
13. pp. I05
between
1975. Phqtophagous
1976. Serengeti
Distribution
lobster abundance. insects as rrgulatorc
wildebeest
migratory
ecological
distribution
12.pp.
I27
of crustacean
herbivores
1976. Some aspects of herbivore-plant
D.. 1975. Plant preference and plant succession. O~~lo~g;r/ R. T. & R. L. V,\IIAS.
1969a. The effects of grazing
0..
on the microflora
34. pp. I:~~I/~I~~I.
seaweed population\.
4q~c/-
food preference. 196’). Bcnthic
on Caribbean
reel\
and \capraa\
(Ed.).
Vol. 18. pp. I2Y
144.
by sea urchms. S~~o,?,ql/oc,c,,rr~ot~c\spp
w
Occw/ro~q~.. Vol. 14. pp 7 I O&719.
Limd.
P.IINF. R. T. & R. L. V~D,%S. 1969b. Caloriflc \hho.
Vol.
fishes and urchins in coral reef commun-
I I1
RI\
.I. UU,UI. l<~~~l/
hiol. ily.5. ( .k..
herbivores
relatlonships
fi/fl,. Ri0/. F&h.. Vol. 3. pp. 4Y 63.
benthic algal populations.
of Itk~rc,~/ (Isopoda).
on cultured
tie\
to invertebrate
flolu by grar~~tz.
136.
beds. Ayf,U//<~ Ho/.. Vol. 7. pp. IO.3 Ilh. O(,r,t v. J. c‘. & P.S. Lonr I 1 197X. The role of herbivorous
P,IIN~.
of energy
of /&~<,rr. ./. ~x,r.
effects of four marine IntertIdal
Vol. 58. pp. 1020-1032. NIC OI 111. M. E.. lY77b. The impact
0
production.
plants. (‘o~rr. ,?u,,‘. .S(I. ( U/I‘. /;,.\
of British spccia
lY55b. The diet and feeding mechanism
O(;DI L. J. C..
and kelp htxis.
of forest primary
: Facilitation
of the epihiota of macroepibenthic
347 355. ‘UICOI KI, M. E.. IY77a. Grazing
U///U,~?. Vol.
sea urchin\,
144.
I OK.E.. lY55a. The Vol. 34. pp. 255 260. IOI<. t..
of herhi-
pp. 92-Y4.
N \\ NI\
importance
pp. 92-94.
S. J..
sc;c/rcx,. Vol
community:
Vol. 29. pp. 603-605.
W. J. & N. D. Aor11.
.S~~i(‘/U.(‘.Vol.
intertidal
abilities. Am. ,‘Vtrr.. Vol. I 12. pp. 2%39.
values of benthic marine algae and their postulated
relation
:Mu~. Bbjl.. Vol. 4. pp. 7Y 86.
algae ah I’ood for some In\ertcbrxrcs
m the inner
part of the Ball c.
I-i,l/frob?S,c,tr. Vol. 7. pp. 2oi- 205.
R>
I HI IN.J. H.. J.C. <;ol IIRIZU, I I,\M\ & 8. E. L.\I~INII.
WII
culture \lstems.
Ci E. <;[I TORI). lY75.
Physical
ily1itrcr1/111~~.Vol. 5. pp. I63
SII HIIKI II. J. Mc N..
.I E.
Hr (8,
models
I \I,\.
A.S.
on integrated
M:I\(,. haste
J.P.
c‘i \,<\I
recycllns
II. I.
marlnc
Il.
polb-
177.
1069. Studies on algal substances 111the ~a.
III.
The production
of c\traccIIuI.Ir
orsr;tntc matter bj Ilttoral marine algae. ./. <‘x-p ,1x/r. H/o/. I!?~~/.. Vol. 3. pp. 311 iO9 Shl I( 11. A. F.. 1926. On the habits and ecology of the tube-building amphipod A/~/>//hoc, ~-f,hr,c~rr~~ Mollt~Lgue.
EuJ/o,ql.
Vol.
7. pp. 4x l--502.