Estuarbte and Coastal 3Iarine Science (I98o) Ix, 593-604

A Comparison o f Reproductive Patterns in Epifaunal and Infaunal Gammaridean Amphipods a

Robert F. Van Dolah S.C. 2$larine Resources Research Institute, P.O. Box 12559, Charleston, ,South Carolina z94tz , U.S.A.

and Edward Bird Department of Zoology, University of ~lraryland, College Park, Maryland eo74e, U.S.A.

Received 5 November I979 and in revised form 24 iffarch 198o

Keywords: Amphipoda; reproduction; eggs; egg weight; epifauna; infauna; Atlantic Ocean northwest

Comparisons of egg size and number are made for xo epifaunal and 16 infaunal species of shallow-water marine or estuarine garmnaridean amphi- pods from the north-western Atlantic. Epifaunal species have significantly more, smaller eggs than infaunaI species of the same size and geographic region. Strong latitudinal and seasonal effects are also evident. For several species, egg size increases and egg number decreases in populations at more northern latitudes and in populations breeding during colder seasons. The few exceptions to the above patterns may reflect unique differences in the biology of particular species. A hypothesis is proposed that adult mortality risk is correlated positively with egg number and inversely with egg size.

Introduction

hiost literature on aquatic invertebrate reproductive patterns is devoted to organisms which release eggs into the environment for pelagic, direct or demersal development (Tt/orson, I95o, 1961 ; Efford, 197o; Sheltema, i97i ; Mileikovsky, I97t ; Vance, i973; Chia, i974; Strathmann, I974). Reproductive fitness for these developmental types, following egg release, is independent of adult survivorship. However, adult survivorship does influence the reproductive fitness of invertebrates which brood their eggs.

One way to increase reproductive fitness in brooding species exposed to a relatively high risk of adult mortality would be to minimize brooding duration. Alternatively, when the risk of adult mortality is low, a beneficial tactic to increase reproductive fitness would be to maxim!ze energy expenditure per offspring to increase competitive fitness (Smith & Fretwell, 1974 ). For many brooding taxa, a greater expenditure of energy per offspring is represented by larger egg size which is directly correlated with longer developmental periods (Steele & Steele, 1975a , c).

~ No. xxz from the South Carolina ~Iarine Resources Center, Charleston, South Carolina z94t2, U.S.A.

593 o3o273S24[8ollzo~q~-blZ $o2.oolo t'~ TORt~ A~-~cl~.~ P.~~ In^ tr ^~.~-~ T ..t

594 R. F. Van Dolah :.~ E. Bird

This paper describes a comparative study on brooding patterns in two groups of gam- maridean amphipods, epifaunal and infaunal species. In general, amphipods are ideal organisms to compare brooding patterns for several reasons: (i) egg development is com- pleted in the brood pouch, (ii) the offspring hatch as juveniles with no metamorphosing larval phase, (iii) the developmental time, life history, and ecology of many species are reported in the literature, and (iv) egg size and number are easily measured. Furthermore, past studies on the ecology of amphipods suggest that infaunal and epifaunal species may be exposed to different mortality risks from predation and]or environmental stresses. For example, Croker (I967) , Dexter (I967) and Sameoto (r969a, b, c) conclude that these factors were not the dominant causes of mortality for several sympatric infaunal species. Rather these studies showed spatial and temporal differences in microhabitat utilization and life histories which presumably were mechanisms to reduce competition, hiany epifaunal species, on the other hand, are subjected to a high risk of mortality, particularly from predation (Vince et al., I976; Van Dolah, i978; Nelson, i978 ). Unfortunately, few comparative studies have documented the relative degree of mortality risk between these two amphipod groups. Nelson (t978 , I979) presents evidence that epifaunal species are subjected to higher mortality from predation than infaunal species in eelgrass beds, but other studies documenting this trend are lacking.

The intent of this paper is to compare reproductive patterns of epifaunal and infaunal amphipods and demonstrate differences between these groups which may be related to a differential risk of adult mortality during brooding. We will present evidence that epifaunal species have relatively smaller eggs, larger broods, and shorter developmental times than infaunal species of comparable size and geographic distribution. The potential advantages of these differences will be discussed.

Methods

Our comparisons are restricted to shallow water marine and estuarine gammaridean species with overlapping geographic ranges in the north-western Atlantic and overlapping mature female sizes, as these factors influence reproductive output (Steele & Steele, I975a, e). The species examined belong to the families Ampeliscidae, Bateidae, Calliopidae, Gammar- idae, Pontoporeiidae, Haustoriidae, Lysianassidae, Melitidae, Oedieerotidac and Phoxo- cephalidae. Amphipods in other groups such as supralittoral, commensal, and epifaunal tube and nest builders are not considered due to insufficient data on their reproductive biology (with respect to egg number, size, and incubation time) or exposure to potential predation and/or competition pressure.

Data were obtained from (i) the literature, (ii) preserved samples from the National gCuseum of Natural History (b,q~NH), Washington, D.C. and (iii) collections during May and June x978, hereafter referred to as the S.C. Collection. Two exceptions include the Maryland sample of Gammarus palustris (Van Dolah, unpublished data) and the Florida sample of .~canthohaustorlus millsi (specimens kindly donated by K. Thoemke, University of South Florida).

For N M N H and South Carolina specimens, the number of eggs were counted in all ovigerous females with undisturbed broods. Stage A egg size and ovigerous female size were also measured as described by Steele & Steele (I969). However, with respect to egg size, we measured four eggs from each of five females whenever possible. Since the criteria used to measure female length has varied among investigators, we compared egg number as a function of female size by adjusting all measurements to total female length (anterior end of

Amphipod reproductive patterns 595

E ~0

,.4

0

o o

N o

2

g

.~ "g

N ~ ~ o

u . ~ ~ u

.~.~

o

~ r~

.o ~.~,_qu >

~u

~ou] ~o- H

o

~ 0 0 ~ ~ 0 0 ~

= 6 ~ G G c ~ G G ~c d~d ~c . 2 ~ o "o ~ o ~ ~ . ~ o o

~ ~ ~ ~ZZVZ ~ ~ ~NZMU o oNZO 3

m m m ~ Z Z M Z ~ M ~ ~

~ 0 0 0 0 0 O ~ 0

~-b~ ~ ~ . t-,y,.,-,

I+1 ~ + 1 /

�9 c - , ~

'u~O t"~N

�9 . .~',-? �9 4'- m ',er ~

N N

v ~ v v v v v v v v v v v

~oo~ ~ ~ ~ P ~ O 0 ~ H ~ o o o ooooo 900 0 0 0 0 0 0 0 . . . . . . .

bbb bbbbbbb ooooo ooo

~ 0 ~ ~ ~ ~ ~ ~

b o o = o o o o o o o = = b b b b b ~ b b b

oo

o

0

r~

t~

2

oO

o o

~e

o u

596 R . F. Van Dolah & E. Bird

o

o

o

0

'-d r .

,-1

0 U~

o~ ~=o'~ .~ "T3

"~ ~3

o

b3

r.o

�9 . 0 0

H ~H c,o o d~o ~o~ u o o o c~c~c~o c~u o

o

M

oo r , . c,,

0 �9 �9 0 0 0

�9 .'.9 ~ P P .

U II I1 II II II II

0 0 0 0 ~ 0 0 0 0 (', ~ 0 0 0 0 0 0 0 ~.~ 0 ~ ' 9 0 ~ " oo 0000090000000000 oo oo

, ~ - H - H ~ - H - H - H - H - H ' H - H - H - H - H - H ' H ' H - H - H ' H ~ ~ ~ ~ ~ ~ - H ' H ~ ~ = ~ - H - H c~ .q- C~ c':. O0 ..d- r~. r... r G~'..O r r N r ' . . r ~ 0 0 r ~ cJ ,d- ~ r

~ b b E b b b b b b b b b b b b b b b b a = = = o o = = = ~~

;o ~-. '-,-, I ~ ,.--, cn ~ c o , . . . . - ~ c n ~ c n . " �9 " " - ~ ' - . " - - ' ~ - . ~ �9 " ~ o �9 " ~ " " , r o r , . ) r O ~ " " . < ~ " " ~ c o ~ < , - , ~ ,-,.~ ,-.~ ro <.-~ . . . . ~ . ~ co..c.ir.j

~'= , , , ~ , . ~ "~ ~

~ ' " ~'a,,~ : ~ ~ ' ~ ~ '~ .~

0

E

o ~

~0

o oo

Q 6 tF

Amphipod reproductive patterns 597

rostrum to tip of telson). Proportions obtained from drawings by Bousfield (x973) were used for those species examined by Dexter (i967, x97I ) and Sameoto (x969b).

Reproductive effort per brood was estimated by calculating clutch volume (CV) for each species in which egg size and number were known. Clutch volume was obtained by multi- plying the average number of eggs]8 mm female (estimated from regression analysis) times egg volume which was calculated using the sphere equation and mean egg diameter.

Results

The compilation of egg size and number for the cpifaunal and infaunal species examined are presented in Tables z and 2, respectively. Although this is not a complete listing of all species which meet our restrictions, it represents all species for which sufficient information was available.

Egg size Comparisons of egg size within species demonstrate strong latitudinal and seasonal effects. In seven species for which we have multiple samples (Gammarus mucronatus, G. obtusatus,

G. palustris, Acanthohaustorius millsi, Ampelisca hohnesi, A. variorum, and Neohaustorlus schrnitzi), egg size is significantly larger in populations collected from more northern latitudes (Tables x, 2; P < o . o I using t-test between each pair of samples). Therefore, comparisons

'rxnlm 3. Comparison of mean size of Stage A eggs for epifaunal and infaunal amphipods from northern and southern sites. See text for restrictions on geo- graphic locations, female size and seasons

Northern Southern

~" Egg size ,~ Egg size Species (ram) Species (ram)

Epifaunal

Infaunal

G. mucronatus o'3x 5 G. mucronatus 0"355 G. mucronatus o-378 G. lawrencianus 0"409 G. stoeremis 0"440 G. tigrinus 0"458 C. laeviusculus o'459 G. obtusatus o'56t G. obtusatus o'6r 4

A. abdita 0"427 A. spinipes 0"459 L. alba 0"5oo A. vadorum o'5x 3 A. holmesi 0"537 A. macrocephala 0"706 A. millsi 0'779 Haustorius sp. 0"946

G. mucronatus (S.C.) 0"296 3I. nitida (S.C.) 0"302 21I. appemtlculata (S.C.) o'3z6 B. cathariensis (S.C.) 0"333 G. palustris (S.C.) 0"342

T. epistomus (S.C.) 0"274 13. parkeri (S.C.) 0"332 P. deichmannae (S.C.) 0"333 A. vadorum (S.C.) 0"372 A. millsi (S.C.) 0"428 A. intermedius (S.C.) 0"434 N. schmltzi 0"454 A. millsi 0"464 A. hohnesi 0"483 N. schmit.~i (S.C.) o'5o2

Mann-Whitney U= x3"5, P < 0"02. Mann-X, Vhitney U (a11)=8"5 P<o'o5 (S.C. samples)=8"5 P<o.xo (S.C. samples excluding T. eplstomus)=

3"5 P<o'o2.

598 R. F. Van Dolah 67? E. Bird

between epifaunal and infaunal species are limited to populations within restricted geo- graphic ranges (Table 3). Northern samples range from Newfoundland to Connecticut and southern samples range from South Carolina to Florida. Since egg size increases during colder seasons (Steele & Steele, z975a; see also Tables z and z), known winter samples were also excluded from the northern and southern comparisons of infaunal and epifaunal species.

In the northern comparison, infaunal species have significantly larger eggs than epifaunal species of similar body size (Table 3). Furthermore, the majority of epifaunal populations examined in this comparison were collected from more northern latitudes than the infaunal populations (Tables z and 2). If all samples had been collected from the same latitude, then differences in egg size would probably have been even greater due to the latitudinal patterns noted within species.

The southern comparison also demonstrates that infaunal species have significantly larger eggs than epifaunal species (Table 3). However, when only South Carolina populations are compared, there is no significant difference between groups (Table 3). This is primarily due to the exceptionally small eggs carried by the infaunal species Trichophoxus epistomus. When 7". epistomus is excluded from the South Carolina comparison (see Discussion), the difference between groups is significant (Table 3).

Similar trends were not apparent for the mid-Atlantic populations. Epifaunal populations of Gammarus palustris and Melita nitida have smaller eggs than the infaunal .4mpelisca vadorum as expected, but larger than the infaunal Amphiporeia virginiana.

Egg number Estimates of egg number versus female size for most species were derived from regression analyses available in the literature (Tables z and 2). Similar estimates were also obtained for six species examined in the NMNH collections (Figures r and 2). Egg number as a function

E 2 ZC i.i

40 1 ' I ~ I e ~ I

l 7 "

�9 o

/ I t . / Y =8.64L-~. -4 ~>

/ / u _ . - - - - ~ ~ 0 ~,.odor,,,. / 9 . - . . . . . . o- r , , ,e~

fJ �9

0 4 t 51 w 61 t 71 T

Ferrde ler~th ~n.rn)

Figure x. Regression of egg number (II) on female length (L) for Gammarus mucronatus from Florida, Illelita nitida from Chesapeake Bay, and Ampelisca vadorum from Rhode Island.

Amphipod reproductive patterns 599

50

40

30

2C

E

w

�9 D

* I J I * I I

f /

M. ed~rardsi 1L ~ / . 4 / Y =3"69 e ~ t" /

r =0"81V~I ~ ~1~

I~ $chmitz[ Y=I'GSL-2.52 / �9 = 0-86 �9 . . . 'b

0 ~ ~ ~ " "r o . .0 " I " A.~,irg/n/a/~a

Y=1"52 L-2'40 r=0.87

* ~ . / - ' o o

0

I 1 I I I | I | I 0 5 4 5 6 7

Femole length (ram)

Figure z. Regression of egg number (I,') on female length (L) for ~lonoculodts e&~ardsi and Neohaustorlus schrnitzi from Georgia, and Arnphi~orela vlrginiana from Maryland.

of female size has not been reported previously for three of the species (Amphlpore?a virgin- iana, 3Iellta nitida, and 3lonoeulodes edwardsi). Two species bad a slightly better fit to a eurvilinear regression rather than a linear regression (Ampelisca vadorum and 3L nftfda). Van Dolah et al. (z975) also found that a curvilinear regression best fit their data on Gam- marus palustris, and this may have been true for other species had larger data sets been available. For all species, egg number increased with increased body size.

Egg numbers of epifaunal and infaunal species were compared at two female sizes (6 and 8 ram) since this size range provided the greatest overlap bet~veen species, and egg number is influenced by female size. The results (Figure 3) include estimates from all populations of every species where this information was available (eight epifaunal species, x 4 populations; seven infaunal species, xx populations) regardless of latitude and season. Despite this lumping, epifaunal species had significantly more eggs at equivalent female sizes (P<o.oo 5 at 6 mm; P<o.o 5 at 8 ram, Mann-Whitney U-test) than infaunal species. If Gammarus obtusatus and Monoculodes edzcardsi [dots below line in Figure 3(a) and dots above line in Figure 3(b), respectively] are excluded from the comparison, the difference in egg number for the remaining species is even more pronounced (P<o.ooi at 6 and 8 mm). Reasons for excluding these species will be discussed later.

Egg number estimates for two infaunal species, Acanthohatutorius intermedius and Proto- haustorhts deiehmannae, were not included in the above comparison due to insufficient data for extrapolation to 6 and 8 mm (Dexter, 1967). However, the egg number for these species (Figure 3(b), intermediate dots at 6.8 and 7"4 mm) is lower than the lowest epifaunal species at 6 ram.

Estimated clutch volumes for eight epifaunal and four infaunal species range from o.4535 to 2.4557 mm a and 0"097 to I'3o77 mm 3, respectively (Tables I and 2). No significant difference in clutch volume was observed between groups (P<o.4o, ~,iann-Whitney U-test).

600 R. F. Van Dolah ~ E. Bird

E 2

2O

,50-

40-

I0

I i I " I I I

(a) epifaunal �9 T (b) infaunol

| |

j,~" ~ f

i " i i j , , ~ ~ 1 d"

�9 ,,,,J / 6 9" ~ o o

0

| 8

8 "" 6

Femo~e lenglh (ram)

Figure 3. Comparison of estimated egg number for (a) epifaunal and (b) infaunal amphipods at two female sizes. Egg number is calculated from the regressions in Tables t and ~. 'The dashed lines are for reference and delineate the exceptions which are discussed in the text.

Discussion

The evidence presented indicates divergent reproductive patterns between amphipod species with different ecological habits. With few exceptions, epifaunal species had smaller eggs and larger broods than infaunal species with a similar adult female size range (Table 3, Figure 3).

The importance of these divergent reproductive patterns is clarified by considering their effect on brood duration. Egg development time is directly correlated with egg size at any temperature. This has been noted for many epifaunal amphipods as well as many other crustacean groups (McLaren, I966; Steele & Steele, x973b, x975c; Wear, x974). Therefore it is reasonable to assume that a similar relationship occurs among all of the amphipod species examined. Based on this relationship, a comparison of egg size between epifaunal and infaunal species indicates that epifaunal species have shorter brooding periods (Table 3).

Among brooding crustaceans, egg size also is inversely correlated with egg number at any given female size (Steele & Steele, 1975a; Kerfoot, x977). Thus, a comparison of egg number between epifaunal and infaunal species of equivalent female size provides an indirect comparison of egg size among species for which only egg number information is available, as well as a direct comparison of egg number between several of the epifaunal and infaunal species examined. The comparatively larger clutch size among epifaunal species (Figure 3) indicates that this group has smaller eggs and therefore shorter developmental times than irffaunal species.

ttmphipod reproductive patterns 601

Only four of the 26 species considered in this study did not conform to the general patterns noted above. These exceptions are most likely the result of our simplifying assumptions. For example, we assumed that all species of the same ecological habit (epifaunal or infaunal) have at least some similarity in the degree of protection from predation and environmental stress. A better approach would be to assess the risk of adult mortality for each species and compare that to their reproductive patterns. Unfortunately, this is not possible with the data currently available.

Two amphipod species demonstrate this problem. Monoculodes edwardsi is an infaunal species, but it probably burrows through the substratum at the mud-water interface with a portion of its body exposed; as do other Monoculodes species (Enequist, x95o; E. L. Bousfield, personal communication). Therefore, its risk of detection by predators is higher than other infaunal species normally inhabiting deeper sediment layers, which may account for the abnormally large number of small eggs observed (Table 2). Amphlporela virginiana is also taxonomically grouped as an infaunal species (Bousfield, x973), but Crokcr (x97o) noted that A. virglniana is 'not as restricted to infaunal living as other haustoriids' and commonly observed large numbers 'swimming in the surf and semiliquid sand' of outer beaches with heavy surf. Thus, the relatively small eggs noted for this species in the comparison of mid- Atlantic populations (Tables x and z) may reflect the effects of unstable environmental conditions.

Differences in life history tactics may explain a third exception to the patterns we note. Trlchophoxus eplstomus is an infaunal species which produces very small eggs (Table z). Although many of the other infaunal species considered in this study are iteroparous (Bousfield, x973), there is evidence that T. epistomus is semelparous (Nelson, x978); a trait often correlated with the production of small, numerous eggs (Stearns, x976 ).

The final exception to our pattern is Gammarus obtusatus. Sexton (1925) stated that (3. obtusatus differs from other species in the time it holds its young. Other Gammarus species he examined release their young within x day of hatching, but G. obtusatus holds its young for extended periods of time, even up to 17 days. The relatively large eggs produced by this species may therefore be the result of additional yolk for young held in the brood pouch after hatching.

There are many potential advantages in having small eggs which develop relatively quickly in high risk environments: (i) Such a pattern increases the chance of successful release of young if predation pressure or unstable environmental conditions increase the probability of adult mortality. Eggs in the brood pouch often make the female more visible to predators since many amphipod species have dark colored eggs even though the adult body is nearly transparent. Furthermore, brooding may require additional energy expenditure (aeration, cleaning) and nutrients (Lawlor, x976 ), making the female less tolerant to other stresses. (ii) Producing small eggs increases tile number of eggs which a female can brood at one time (Steele & Steele, x975c ). This can be advantageous when risk of adult and/or juvenile mortality is high (see Price, x974; Thompson, x975; Stearns, I976 ). (iii) Having smaller eggs and therefore a relatively quick incubation time, may increase the number of broods in a reproductive season (Steele & Steele, x975c ). (iv) Since egg size also is correlated with size at maturity in amphipods (Steele & Steele, i975a), producing smaller eggs may decrease the time to maturity which in turn would increase the intrinsic growth rate of the population. (v) Finally, when size-selective predation increases the risk of mortality to large adults, the production of small eggs somewhat alleviates the disadvantage of selection for small females which produce fewer eggs per brood. For example, Strong (I97Z) demonstrated that populations of IIyallela azteca which experience high adult mortality from predation had

6oz R. F. Van Dolah 6Y E. Bird

shorter periods of amplexus and smaller females than populations in a predation-free environment. Although these females produced fewer eggs per brood, egg size was small and incubation times were shorter for the populations from a high risk environment. Belk (x977) also showed that fairy shrimp in unstable environments produced more numerous small eggs than fairy shrimp in more stable environments.

In contrast, there are several potential advantages to producing fewer, larger eggs in a relatively stable environment with a low risk of adult mortality: (i) Producing larger eggs results in larger young at the time of release into the environment (Steele & Steele, x975c), which is often correlated with increased fitness of the young (Thorson, r95o; Price, I974; Smith & Fretavell, x974; Strathmann, x977). (ii) Producing larger eggs increases size at maturity (Steele & Steele, x975c ) and possibly competitive ability. Larger species (Menge & Bfenge, x974; Nagle, x968 ) and larger individuals within a species (Borbjerg, x956; Connell, x963) are often dominant in aggressive encounters and are possibly better competitors. (iii) Although adult mortality is low, there may still be strong predation pressure on juveniles. Therefore, the production of larger offspring might alleviate juvenile mortality as noted in other organisms (Kerfoot, x977). (iv) Finally, it is possible that larger juveniles must be produced for some infaunal amphipod species to survive in coarse-grained sand environ- ments. Increased juvenile size could prevent damage from shifting sands, allow effective locomotion, or increase water retention to avoid desiccation.

Based on r- and K-selection theory ~'IacArthur & Wilson, I967; Pianka, x97o), epifaunal amphipods might be expected to devote more total energy to reproduction than infaunal species since the former generally inhabit higher risk environments. However, we observed no significant difference in clutch volume between the infaunal and epifaunal species tested and the majority of species in both groups are annual and iteroparous (Bousfield, x973). Therefore, infaunal and epifaunal species appear to devote approximately equal amounts of energy to reproduction but with divergent patterns.

The general reproductive patterns we observed may be common among other brooding species. For example, in a concurrent but unrelated study of amphipod reproductive patterns, Nelson (x98o) has also obtained evidence that epifaunal species have significantly greater brood sizes than infaunal species. This evidence, combined with his previous observations that predation pressure is greater on epifaunal versus infaunal species (Nelson, r978, x979) strongly supports our results. More rigorous tests are needed, particularly among species reproducing at equivalent latitudes and seasons combined with conclusive evidence of differential risk of adult mortality. This latter point is especially important since there is growing evidence that some infaunal communities are regulated by predation (Reise, x976; Orth, x977; Virnstein, r977; Schnieder, i978). However, it is possible that producing numerous small eggs with short incubation periods is common among brooding invertebrates inhabiting high risk environments as compared to invertebrates inhabiting environments with a lower risk of adult mortality.

Acknowledgements

We wish to thank D. Allan, J. Barnard, S. Bell, E. Bousfield, D. Calder, J. Grant, W. Nelson, M. Reaka, P. Sandifer, S. Stancyk and R. Virnstein for their comments and constructive criticism of this manuscript. ~lany of the South Carolina specimens examined were from samples collected for Contract No. DACW6o-77-C--oox 3, funded by the U.S. Army Corps of Engineers, Charleston District; and Contract No. W74RDV CERC 77-59, funded by the U.S. Army Coastal Engineering Research Center, Fort Belvoir, Virginia. D. Knott aided in

Amphlpod reproductive patterns 603

the collection, sorting and identification of many infaunal species. In addition, we thank

J. Barnard for making the N M N H collection available to us.

References

Belk, D. z977 Evolution of egg size strategies in fairy shrimps. Southwestern Naturalist 22~ 99-x05. Bousfield, E. L. x973 Shallow-water Gammaridean Amphlpoda of New England. Cornell University

Press, Ithaca. 3z2 pp. Borbjerg, R. V. z956 Some factors affecting aggressive behavior in crayfish. Physiological Zoology 29~

z27-z36. Chia, F. S. x974 Classification and adaptive significance of developmental patterns in marine inverte-

brates. ThalassiaJugoslavlca zo, xex-x3o. Connell, J. H. z963 Territorial behavior and dispersion in some marine invertebrates. Researches on

Population Ecology 5, 87-zox. Croker, R. A. x967 Niche diversity in five sympatrie species of intertidal amphipods (Crustacea:

Haustoriidae). Ecological Monographs -37~ x73-zoo. Croker, R. A. x97o Intertidal sand macrofauna from Long Island, New York. Chesapeake Science zz,

z34-x37. Dexter, D. I~I. z967 Distribution and niche diversity of haustoriid amphipods in North Carolina.

Chesapeake Science 8, x87-x9z. Dexter, D. M. x97z Life history of the sandy-beach amphipod Neohaustorius schmltzi (Crustacea:

Haustoriidae) Marbze Biology 8~ 232-237. Efford, I. E. z97o Recruitment to sedentary marine populations as exemplified by the sand crab Emerita

analoga (Decapoda, Hippidae). Crustaceana zS~ z93-3o8. Enequist, P. z95 o Studies on the soft bottom amphipods of the Skagerak. Zoologlska Bidrag Fran

Uppsala 28, z97-49z. Kerfoot, W. C. z977 Competition in cladoceran communities: The cost of evolving defenses against

copepod predation. Ecology 58, 3o3-3x3. Lawlor, L. R. z976 Parental investment and offspring fitness in the terrestrial isopod Armadillidium

vulgare (Latr.) (Crustacea: Oniscoidea). Evolution 3o, 775-785. MacArthur, R. H. & Wilson, E. O. z967 The Theory oflslandBiogeography. Princeton University Press,

Princeton. zo3 pp. NIcLaren, I. A. z966 Predicting development rate of copepod eggs. Biological Bulletin I31, 457-469. l~ienge, J. L. & l~,ienge, B. A. z 974 Role of resource allocation, aggression, and spatial heterogeneity in

coexistence of two competing intertidal starfish. Ecological ~Ionographs 44, z89-zog. Mileikovsky, S. A. z97z Types of larval development in marine bottom invertebrates, their distribution

and ecological significance: A reevaluation. Marine Biology zo, x93--2z3. l~iills, E. L. z967 The biology of an ampeliscid amphipod crustacean sibling species pair.Journal of the

Fisheries Research Board of Canada 24, 305-355. Nagle, J. S. z968 Distribution of the epibiota of macroepibenthie plants. Contributions in Marbze

Science, University of Texas Marine Institute x3, zos-z44. Nelson, W. G. z978 The community ecology of seagrass amphipods: Predation and communiW

structure, life histories, and biogeography. Ph.D. Thesis, Duke University, Durham. zz3 pp. Nelson, ~,V. G. z979 An analysis of structural pattern in an eelgrass (Zostera ntarina L.) amphipod

community. Journal of Experimental Marine Biology attd Ecology 39, z3 z-z64. Nelson, ~V. G. z98o Reproductive patterns in gammaridean amphipods. Sarsia 65~ (in press). Orth, R. J. z977 The importance of sediment stability in seagrass communities. In Ecology of 2~Iarbte

Benthos (Coull, B. C., ed.). University of South Carolina Press, Columbia, S.C. pp. z8z-3oo. Pianka, E. R. z97o On r- and K-selection. American Naturalist xo4, 59z-597. Price, P. ~V. z974 Strategies for egg production. Evolution 28~ 76-84. Raise, K. x976 Predation pressure and community structure of an intertidal soft-bottom fauna. In

Biology of Benthic Organisms (Keegan, B. F., Ceidigh, P. O. & Boaden, P. J. S., eds). Pergamon Press, New York. pp. 5z3-5z9.

Sameoto, D. D. z969a Comparative ecology, life histories, and behavior of intertidal sand-burrowing amphipods (Crustacea: Haustoriidae) at Cape Cod. Journal of the Fisheries Research Board of Canada 26~ 36z-388.

Sameoto, D. D. z969b Some aspects of the ecology and life cycle of three species of subtidal sand- burrowing amphipods (Crustacea: Haustoriidae). Journal of the Fisheries Research Board of Canada 26~ z3az-z345.

Sameoto, D. D. z969c Physiological tolerances and behaviour responses of five species Haustorlidae (Amphipoda: Crustacea) to five environmental factors. Journal of the Fisheries Research Board of Canada z6~ zz83-zz98.

604 R. F. Van Dolah & E. Bird

Scheltema, R. S. 197r Larval dispersal as a means of genetic exchange between geographically separate populations of shallow-water benthic marine gastropods. Biological Bulletin 14% 284-31z.

Schnieder, D. 1978 Equalization of prey numbers by migratory shorebirds. Nature z7x~ 353-354. Sexton, E. W. 19z5 The moulting and growth-stages of Gammarus, with descriptions of the normals

and intersexes of G. cheureuxi, ffournal of the lllarine Biological Association of the United Kingdom 13, 34o-4ox.

Smith, C. C. & Fretwell, S. D. 1974Tl'/e optimal balancehetweensizeand numberof offspring. American Naturalist xo8~ 499--506.

Stearns, S. C. x 976 Life history tactics : A review of the ideas. The Quarterly Review of Biology 51~ 3-47. Steele, D. H. & Steele, V. J. x 969 The biology of Gammarus (Crustacea, Amphipoda) in the northwestern

Atlantic. I. Gammarus duebeni LilIj. Canadian ffournal of Zoology 47, 235-144. Steele, D. tI . & Steele, V. J. 197oa The biology of Gammarus (Crustacea; Amphipoda) in the north-

western Atlantic III . Gammarus obtusatus Dahl. Canadian ffournal of Zoology 48~ 989-995. Steele, D. H. & Steele, V. J. 197ob The biology of Gammarus (Crustacea, Amphipoda) in the north-

western Atlantic. IV. Gammarus lawrencianus Bousfield. Canadian ffournal of Zoology 48~ 1961-1267. Steele, D. tI . & Steele, V. J. 1972 The biology of Gammarus (Crustacea, Amphipoda) in the north-

western Atlantic. VI. Gammarus tlgrinus Sexton. Canadianffournal of Zoology 50, xo63-xo68. Steele, D. H. & Steele, V. J. 1973 a Some aspects of the biology of Calliopius laeviuscolus (Kroyer)

(Crustacea, Amphipoda) in the northwestern Atlantic. Canadianffournal of Zoology 51b 723--728. Steele, D. It. & Steele, V. J. 1973b The biology of Gammarus (Crustacea, Amphipoda) in the north-

western Atlantic. VIII . The duration of embryonic development in five species at various tempera- tures. Cmmdian ff~urnal of Zoology 51~ 995-999.

Steele, D. H. & Steele, V. J. 1975a The biology of Gammarus (Crustacea: Amphipoda) in the north- western Atlantic XI. Comparison and discussion. Canadlan ffournal of Zoology 52~ z t 16--x 126.

Steele, D. H. & Steele, V. J. 1975b The biology of Gammarus (Crustacea, Amphipoda) in the north- western Atlantic. IX. Gammarus wilkitzkii Birula, Gammarus stoerensis Reid, and Gammarus mucronatus Say. Cam~dlan~ournal of Zoology 53~ x xo5-1 xo9.

Steele, D. H. & Steele, V. J. 1975 c Egg size and duration of embryonic development in crustacea. Internationale Rewte der gesamten Hydrobiologie 6o~ 711--715.

Strathmann, R. R. 1974 The spread of sibling larvae of sedentary marine invertebrates. American Naturalist IO8, 29-44.

Strathmann, R. R. 1977 Egg size, larval development, and juvenile size in benthic marine invertebrates. American Naturalist xlx~ 373-376.

Strong, D. R. Jr. 1972 Life history variation among populations of an amphipod (tlyalella azteca). Ecology 53, xxo3-txxt.

Thompson, J. N. 1975 Reproductive strategies: A review of concepts with particular reference to the number of offspring produced per reproductive period. The Biologist 579 x4-25.

Thorson, G. 195o Reproductive and larval ecology of marine bottom invertebrates. Biological Bevierz's 25, r-45.

Thorson, G. 1961 Length of pelagic larval life in marine bottom invertebrates as related to larval transport by ocean currents. Oceanography. American Association Advancement of Sciences. Publ. No. 67j 455-474.

Vance, R. R. 1973 On reproductive strategies in marine benthic invertebrates. American Naturalist IoTj 339-352.

Van Dolah, R. F., Shapiro, L. E. &Rees, C. P. I975 Analysis of an intertidal population of the amphipod Gammarus palustris using a modified version of the egg-ratio method. 3Iarine Biology 33, 323-33o.

Van Dolah, R. F. I978 Factors regulating the distribution and population dynamics of the amphipod Gammarus palustris in an intertidal salt marsh community. Ecological 3fonographs 48, 191-217.

Vince, S., Valiela, I., Backus, N. & Teal, J. M. 1976 Predation by the salt marsh killifish Fundulus heteroclitus (L.) in relation to prey size and habitat structure: Consequences for prey distribution and abundance, ffonrnal of Experbnental 2$larhze Biology and Ecology 13, 255-266.

Virnstein, R. W. 1977 The importance of predation by crabs and fishes on benthic infauna in Chesa- peake hay. Ecology 58, 1199-1217.

Wear, R. G. 1974 Incubation in British decapod Crustacea and the effects of temperature on the rate and success of embryonic development, ffournal of the 2$Iarine Biological Association of the United Kingdom 54, 745-761.