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Evolutionary ecology of
reproduction in gammaridean
Amphipoda
a
D. J. Wildish
a
Fisheries and Environmental Sciences, Department
of Fisheries and Oceans , Biological Station , St.
Andrews, New Brunswick , EOG 2XO , Canada
Published online: 10 Sep 2012.

To cite this article: D. J. Wildish (1982) Evolutionary ecology of reproduction in

gammaridean Amphipoda, International Journal of Invertebrate Reproduction, 5:1,
1-19, DOI: 10.1080/01651269.1982.10553450

To link to this article: http://dx.doi.org/10.1080/01651269.1982.10553450

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 International Journal of Invertebrate Reproduction, 5 (1982) 1-19
Elsevier Biomedical Press

Review article

Evolutionary ecology of reproduction in

gammaridean Amphipoda
D.J. Wildish
Fisheries and Environmental Sciences, Department of Fisheries and Oceans, Biological Station, St. Andrews,
New Brunswick EOG 2XO, Canada
Downloaded by [University of Glasgow] at 08:46 03 January 2015

(Received 9 July 1981)

A classification of amphipod life histories is proposed inclusive of six categories: multivoltine

semi-annual, uni- or multivoltine annual, semelparous biannual and semelparous or iteroparous perennial:
this should accommodate unknown, as well as known, life histories. The life history diagram is suggested
to be the most accurate way of communicating life history data.
Life histories of the few studied annual, and biannual gammaridean Amphipoda are characterized by
early maturity with a short growth and reproductive period. Body size is the major controlling factor for
reproductive effort and adjustments of growth rate and time of brood production are adaptive in
regulating life histories. The adaptations are typical of environmental conditions where unpredictable
physical factors influence mortality. Semiannual life histories of Gammaridea, by contrast, are associated
with tropical conditions or influenced by predation pressure. The greatly increased reproductive potential
involved is not a physiological cost to a single female because multiple generations are produced, made
possible by increased growth rate and shorter generation times.

life history: reproductive potential: Amphipoda: Gammaridea

Introduction

Throughout the Invertebrata, sexual reproduction fulfills two key functions:

production of new recruits and genetic variants,· enabling the process of natural
selection to occur at a rate comparable to or greater than the rate of change of the
environment.
Although a diversity of reproductive methods is found in the class Crustacea [1],
most gammaridean Amphipoda are dioecious with internal fertilization and lecitho-
tropic eggs. The eggs are carried in a marsupium, or brood pouch, formed from
leaf-like, setose outgrowths or oostegites from the bases of the peraeopods.
This review considers literature relating to the evolutionary adaptations and
ecology of reproduction in gammaridean Amphipoda. Previous reviews of some
aspects of this subject have been made by Steele and Steele [2] on marine Gammarus
and by Morino [3] on Orchestia platensis. Nelson [4] presents a correlative study of
life history characteristics versus mode of life, environmental factors, and familial
groupings in Gammaridea.

0165-1269j82j()()()()-0000j$02.75 © 1982 Elsevier Biomedical Press

 2

Measurement of reproductive resources

The development of measures for the deployment of reproductive resources

depends upon the purpose of the analysis. Of concern here is the presentation of
observational and experimental data useful in comparing the reproductive adapta-
tions of Gammaridea. Two considerations are of prime importance: standardization
and simplification. The realization of this view must take into account the relatively
little work done so far and the belief that only by the use of uniform measures
applied to a number of taxonomically divergent groups will it be possible to develop
comparative data useful for the purposes mentioned.
Statistics measuring the reproductive effort as numbers of births minus natural
mortality, such as the innate capacity for increase (r"' ), or the capacity for increase
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( rc) of Andrewarthra and Birch [5]. or the birth rate (b) of Van Dolah and Bird [6].
will not be used here. In few amphipod species have the necessary survival and
fecundity life table data been gathered. Instead. a simpler measure. R. the reproduc-
tive or biotic potential which does not account for natural mortality will be used:
R=hnp (I)
where R is the total number of reproductive units produced per unit time
(numberjyear), b is the number of eggs per brood, n is the number of broods per
individual female per year (voltinism: uni- or multivoltine; indicating one or more
than one brood per year, respectively), and p is the proportion (0- I) of adult females
in relation to the total adult male and females present. Because of the marked effect
of generation time on biotic potential [7] in terms of total numbers and rate of
reproduction, R has been modified ( R max) to account for the case where overlapping
generations occur:
R max = R generation I + X R generation 2 •• +X R generation. ( 2)

where g is the maxin:tum number of breeding generations found per year and X is the
maximum potential number of females giving rise to the appropriate generation.
This expression requires knowledge of both generation time and longevity and yields
a potential number of young which may be much higher than actuality because the
calculations do not account for females which die before breeding. Species with
generation times less than 0.5 yr will have two or more generations per year and are
referred to as multivoltine semiannual species. Annual species, on the other hand,
have a single generation per year with generation/longevity times of 0.5-1.5 yr and
one or more broods per year. Other species which do not reproduce until the second
or later years, that is with· generation/longevity times in excess of 1.5 yr, are
accordingly referred to as biannual ( > 1.5-2.5 yr) or perennial forms ( > 2.5 yr).
The physiological 'cost' of reproduction to an individual cannot be measured
adequately by numbers alone and recourse must be made to a measure of energy
content of the individual at the agejsize a brood is first produced in relation to the
energy content of the brood [8]. This can be expressed as the reproductive efficiency
( Erp) of an individual in terms of energy as defined by Saito [9]:

(3)
 3

where heal is the total energy content in calories of the brood just after laying and /cal
is the total energy content, in the same units, of the female just after release of the
ova. If the reproductive efficiency remains constant for successive broods, or for
semelparous species, the reproductive energy ratio ( TErp) is obtained by substituting
in Eqn. I with omission of the sex ratio term, thus:
(heal · 11 )
TErp = /cal + (heal · 11) X 100 (4)

For many iteroparous species, however, the calculations must be repeated for
each brood because one or more of the terms may change with time, for example,
seasonal changes in brood numbers. According to Tinkle and Hadley [8]. full
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consideration of the evolution of reproductive effort requires knowledge of the

parental energy budget inclusive of maintenance and growth energy costs. Construc-
tion of an energy budget requires considerable time and effort and little work of this
kind has been attempted yet for any Crustacea. The simpler measures proposed here
will provide a better starting point for the comparative assessment of reproductive
'costs'.
Because virtually no energetics data are available, a simplified cost measure has
been devised for this study. Thus, the total egg volume in a brood is:
4j37Tr 3 ·h (5)
where r is half the length of an average egg. The proportion of the total available egg
volume devoted to each egg is mathematically equivalent to the inverse of the brood
number [I 0]. An estimate of the volume of a brood carrying female is made as
follows:
( 6)

where L is the body length of the female from the tip of the telson to the anterior
part of the cephalon in mm, and dis the body depth (in mm) at the third peraeon
segment. The reproductive cost (%RR) to an individual amphipod can then be
expressed as:
(4/J 7Tr 3 b)
%RR = X 100 (7)
7Td 2 • L

Life history

Known amphipod life histories are of three basic types (Fig. 1), the most common
being the annual with either single (semelparous) or multiple (iteroparous) broods
produced during the life history. The semiannual life history is derived from the
annual one, occuring when growth and sexual development rates are increased to the
point where young produced early in the year mature during the same year and yield
a second, or more, generations during that year. The calculations for Rmax in Table I
are made in the following way, using Crangonyx gracilis as an example:
 4

Semi-annual Annual BI-annual

Year Month
Qflll'!'mereffua P. femorete C. bigetowi
Jon
Feb.
Mar
Apr.
May
June
July
Aug.
Sept.
Oct.
Nov.
Dec
Jon.
Feb.
Mar.
Apr.
May
2 June
July
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Aug.
Sept.
Oct.
Nov
Dec.
Jon
Feb.
Mar
Apr
May
June
3 July
Aug.
Sept
Oct
Nov
Dec.

Fig. I. Life-history diagrams of 0. gammarellus, Medway estuary, Great Britain; Pontoporeia femoral a, St.
Margarets Bay, Canada; Casco bigelowi, Digedguash estuary, Canada. Circles indicate brood production,
lines embryonic development, bars post-embryonic development, unshaded bar juveniles, stippled bar
immature, left-sloping hatching mature and right-sloping hatching period of sexual quiescence.

R generation 1 = 83
33 X 5 X 0.5
X( R generation,,,) = 15(33 X 3 X 0.5) = 743
X ( R generation ,h ) = 15(33 X 2 X 0.5) = 495
X( R generation,, ) = 15(33 X I X 0.5) = 248

The value of X used is that suggested by Hynes [ 12) for this population and the total
of 1569 differs from that quoted by this author because of the correction for sex
ratio applied in the calculation. In Fig. 2. different numbers are used to refer to
different generations that differ in female (always) and male (often) parents and
different letters to designate successive broods from the same female but (often) a
different male parent. Populations with more than two generations per year are
known; thus the summer. seasonal breeder. Hyalella a=teca in North America. has a
generation time of 7-9 weeks [ 14] and hence at least 3-4 generations per year.
although a population of this species breeding year round in hot springs [ 15) could
have at least seven generations per year. Steele (16) has reported a tropical hyalellid.
Parahyallela pietschmanni, living at latitude 13° S with a generation time of 5 weeks
and year-round breeding and hence at least 10 generations per year. Since this
 Downloaded by [University of Glasgow] at 08:46 03 January 2015

TABLE I
Reproductive potential for amphipoda with a semiannual life history

Species Length Mean egg Generation h , p R R rna:~ Reference

(mm) diameter
(mm) No. Duration (yr)

Talitridae
Orchestiu gummurellus 12-IR I 0.7 19 7 0.50
O.R2 679 } 153 II
2 0.5 19 I 0.50
0. plutensis 0.69 I 0.7 14 3 0.50
0.59 2a 0.3 4 7 0.50 14 J
2l 3
7-12 0.59 2b 0.3 4 7 0.50 I~ l _73
0.66 2c 0.2 4 4 0.50
Gammaridae
Gumnwrus pulex 6-12 I 0.3 16 6 0.50 4R}
2 16 2 0.50 16 160
G. fusciutus 6-13 I 29 4 0.50
12
2a 29 3 0.50 44
2b - 29 2 0.50 "
29 \ 1276 I
2c 29 I 0.50 14
Crungonrx gracilis 6-10 I - 33 5 0.50
2a - 33 3 0.50
12
2b - 33 2 0.50 l!\15691
2c 33 I 0.50
Gummurus luwrencianus 5-10 I 24 7 0.50 4
R } 516
0.41
2 24 3 0.50
G. tigrinus 7-13 0.46 I 35 7 0.50 123
} 1016 ~ 2
2 35 3 0.50
G. stoerensis 5- 7 I II 7 0.50
94
0.44
2 II 2 0.50 II
"l V>
 6

Sample
Month Generation

2a
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2b

2c

Fig. 2. Life-history diagram of Crangonrx richmondensis lauremianus, Lillie Minnow Lak~. Canada. based
on data from Sprules [ 13].

TABLE II
Reproductive potential ( R) for some amphipod populations with an annual life history

Mean Mean egg h II p R Reference

~ ~ diameter
length (mm)
(mm)
Talitridae
Orchestia cat•imana 16 0.69 IR 6 0.50 46
0. remyi roffensis R 0.62 5 4 0.7g 17
II
0. mediterranea
mediterranea 20 0.72 36 5 0.50 !!3
0. mediterranea
aestuarensis 20 0.72 36 4 0.67 96
Gammaridae
Gammarus
wilkirzkii 20 0.73 90-250 I 0.50 45-125
G. setosus 14 0.69 20-250 I 0.50 10- 75
G. ohrusatus g 0.65 17 3 0.50 25
1
G. oceanicus 14 0.55 90 3 0.50 135
G. finmarchicus II 0.50 30 g 0.50 120
G. dueheni 12 0.57 40 5 0.50 100
G. dueheni 19 5 0.67 64
G. lacustris 15 22 5 0.50 55 } 12

Aoridae
Leptocheirus
pinguis 16 0.53 51 0.50 26 10
 7

species is multivoltine, the potential reproductive output is large.

That growth is faster and generation times shorter in semiannual populations can
be appreciated by comparing the generation times in Table II with those of annual
(0.5-1.5 yr) and biannual ( 1.5-2.5 yr) populations. The data of Table I are limited to
studies, which include field population analysis as well as a laboratory study of
multivoltine species to determine the generation time, number of broods which can
be produced free of natural mortality, and development rates. Studies based on field
population analysis only, as for example that of Williams [ 17) on Tulitrus sultator,
may result in an underestimation of the number of broods potentially available in a
year.
Amphipod populations with an annual life history may be uni- or multivoltine
(Table II), and in such populations the annual energetic cost of reproduction is
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borne by females from one generation. By contrast, the high annual reproductive
potential of semiannual populations is achieved by females from two, or more,
generations. Biannual populations (Table III) so far known are semelparous. In the
biannual Ampeliscidae, the male undergoes a terminal molt to maturity after which
he undertakes a short-lived, pelagic phase functional in gene dispersal for this
sedentary. tube-living family.
The adoption of a particular life history shown in Fig. I does not appear to be a
fixed feature within a given species, and local and geographic variants are probably
commoner than the available literature suggests. Life history variations have been
described for Gummurus dueheni which is semiannual in fresh water and annual in
brackish water of the British Isles [20]. Wiederholm [21) describes a multivoltine
annual life history for Pontoporeiu a/finis in the shallow, eutrophic, western end of
Lake Malaren, Sweden. and a semelparous biannual one in the deeper, less eutrophic.

TABLE III
Reproductive potential ( R) for some amp hi pod populations with a biannual life history

Mean Mean egg b n p R Reference

~ ~ diameter
length (mm)
(mrn)

Ampeliscidae
Hap/oops fundiensis 7 0.47 5 0.5 0.50 I (Wildish, unpublished)

I~}
H. tenuis 8 0.66 35 0.5 0.50
18
H. tubicola 10.5 0.84 45 0.5 0.50
Ampelisca
macrocephala 16.5 0.80 60 0.5 0.50 15 19
Melitidae
Casco bigelowi
( 5 m) 19.5 0.69 50 0.5 0.50 13 } 10
(80m) 15.0 0.69 40 0.5 0.50 10
 8

10000[ A

1\
1000'- \
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•
'
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\
\ \'-----------.----~
N

.....
E

.
0
\ o-.....:o:....__ _o""'

..... \
\
• 0

.·~-----------.
~
z
.
Downloaded by [University of Glasgow] at 08:46 03 January 2015

' I
I
I
I
I

~0
I
I
I
I
I
I
I

IMl-~-L--AL-~5--~0~NL-~D--L-~~M--~A~M~~~~~A
Samplinq Dale

N
E
\
....;
"
\
j 100
~
z

10

Samplinq Date

Fig. 3. Mortality curves ror (A) Pomoporeia femorata rrom St. Margaret"s Bay. Canada: (B) Corophium
volutator. Bay or Fundy. Canada. From unpublished data or D. Peer and D.J. Wildish.
 9

central basins of this lake. Semiannual species which produce two generations per
year in the more southerly part of their range, for example 0. gammarellus and
0. platens is (Table 1), probably are annual near the northern range limits.
A feature of some annual and semiannual life histories at high latitudes is the
presence of a resting stage or period of quiescence in female reproductive behaviour
[22,23]. A resting stage entails cessation of oogonial development and a concomitant
loss of the characteristic fringing setae on the oostegites.
A resting stage is characteristic of seasonal breeders such as Gammarus and
Orchestia which may separate broods borne in two successive growing seasons. In
Gammarus wilkitzkii and G. setosus, however, there is an obligatory resting stage
following brood production which ensures that only a single brood is produced per
year [2,24,25]. The functional significance of sexual quiescence seems to be linked to
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the need to release the post-emergent hatchling at the most appropriate time for
successful foraging when the growing season is limited.

Environmental factors controlling reproduction

Wilbur et al. [26] pointed out that a number of environmental driving forces,
inclusive of the density of the population in relation to resources, the trophic and
successional position of the population, and the predictability of mortality patterns.
are required to explain life-history strategies.
Considering the density of amphipod populations in relation to environmental
resources, Wildish [27] recognized two paradigms based on the r and K concept of
MacArthur and Wilson [28]. Where environmental resources such as food and
shelter are not limiting, as seems to be the case with many intertidal amphipods, the
ecological genetics homeorheostat [27] is in operation and demes are the units
undergoing selection towards maximum numbers and rates of reproduction.
Trophically, only a few of the Gammaridea are predators or parasites and the
majority are either macrophagous, utilizing macroalgae, detritus, and carrion, or
microphagous filter- or deposit-feeders utilizing microflora and detritus [29]. Gam-
maridea have been shown to rapidly expand their population numbers as a result of
enrichment from organic pollution [30] consistent with the belief that they are
primarily r-selected.
Mortality data are not available for most species and from the few where
mortality is reasonably well known (Fig. 3) the following is apparent. There is high
juvenile mortality; a timejsize dependent, senescent mortality of adults; and in one
cohort of the semiannual, C. volutator, individuals reaching a minimum size were
heavily predated by the semipalmated sand piper during the few months in summer
when this wader was present on the shore (D. Peer, personal communication).

Physical factors

Temperature
Life-history adaptations by ten species of intertidal, manne Gammarus, were
 10

shown by Steele and Steele [2] to be the reason that Gammarus occupied such an
extensive geographic range (from the North Pole to the Gulf of Mexico in the
northwest Atlantic). Temperature through its control of metabolic rate, body size,
and linked effects on reproductive effort was the fundamental forcing function for
the life history adaptations found. Thus the northern species, G. wi/kit:::kii and G.
setosus, grew to a large size and delayed brood production until a single, annual
brood was produced at a time which allowed juveniles to feed in the short growing
season of high latitudes. By contrast, more southern species of Gamnwrus, such as
G. lawrencianus, G. tigrinus, G. stoerensis, and G. mucronatus, grow quicker, mature
earlier, produce a large number of small broods in a longer growing season, and may
produce second generations in a year. Experimental evidence for the importance of
temperature on reproductive bionomics is provided by Steele et al. [23]. The obvious
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importance of temperature has led Morino [3] to suggest that the distinctive life
history classes are characteristic of specific climatic zones of the world - thus
biannual species in polar and cold temperatures, annual in temperate, and semian-
nual in tropical regions. This generalization cannot be more rigorously examined
because of our poor knowledge of the life history and reproductive bionomics of
tropical species. Two tropical species; P.pietschmanni [16] and Melita zeylanica [31],
are both semiannual and breed throughout the year. A universal relationship might
involve mean ambient temperature and the reproductive potential (R, see Eqn. 1).
Thus, continental slope and abyssal amphipods could be included in such a scheme
although, at present, little information regarding them is available.

200~------.-------.-------.-----~/

/
/

ISO

i:IOO
<:>:::

50

0 25 50 75 100
p
Fig. 4. Theoretical relationship between adult sex ratio. p. and reproductive potential R. in polvgvnou>
amphipod populations [34]. Both p and R are given as percentages.
 II

Salinizv
Low salinity has been shown to be a powerful selection factor in estuaries. Thus,
in a British estuary, the median lethal concentration of dilute seawater to Orchestia
Kammarellus near seasonal extremes, 4 and 23°C, was 0.4-1.8%a chlorinity which
was near the field-observed, limiting isohaline at high water of l-2%a Cl- [32]. The
direct lethal effect of low salinities during dispersal could explain the range limit of
0. Kammarellus in estuaries. However, in another marine species, 0. mediterranea,
the upstream limiting mean chlorinity was 5- 7%a and the median lethal concentra-
tion was 0.5-2.4%a o-, suggesting that a lethal limiting mechanism is not the only
answer. Breeding experiments at different chlorinities show that at sublethal low
chlorinities reproductive success is curtailed by increasing the intermolt period,
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decreasing the breeding season and increased female mortality; all attributable to
the additive physiological costs of reproduction and osmotic stress [33 J. In response
to these effects in estuaries. 0. mediterranea produces a polymorphic form,
aestuarensis, with female-biased broods (monogeny) of value to the deme in in-
creasing R or Rmax• as is explained below, and which is possibly better able to
tolerate low salinities in estuaries.
That sex ratio can have a marked effect on R or R max can be shown theoretically
(Fig. 4). The relationship applies where mating systems are polygynous, a condition
which probably applies to most amphipods. The categories of R recognizable in
Fig. 4 are:
(I) R% depends on a limiting proportion of females and possibly the intensity of
male competition for mates which may further reduce R;
(II) R% depends on the proportion of females present and may involve increases or
decreases greater than 50% of the equal sex ratio condition;
(Ill) R% depends on a limiting proportion of males available for mating with
females and possibly on female competition for mates which may further
reduceR.

The controlling mechanisms of monogeny have not been convincingly demon-

strated in amphipods. Two hypotheses compatible with the facts are that sex bias is
genetically controlled or that endoparasitic infections produce a feminizing effect in
genetic males resulting in a change to intersex or female status. The infection is
passed from generation to generation via the egg. Gammaridean amphipods where
monogeny is suspected include 0. remyi roffensis [II], 0. mediterranea aestuarensis
[33], and 0. gammarel/us [34].
The basis of monogeny in 0. mediterranea is thought to be genetic involving two
morphs which are selected by the salinity conditions experienced [33]. Interestingly,
the cross male mediterranea X female aestuarensis is virtually sterile and male
mediterranea immigrants to an aestuarensis colony would be unable to alter gene
frequencies; whereas the reciprocal cross is fertile. Definitive genetic experiments
which could separate genetic and parasitic causes of monogeny are not available.
Ginsberger-Vogel and Desportes [35] have described an endoparasite in some
populations of 0. gammarellus, the haplosporidian Marteilia sp., which produces a
temperature sensitive feminizing effect. The direct evidence as to how the endopara-
 12

site causes the feminizing effect is not available. Bulnheim [36] originally described
endoparasitic microsporidians in amphipods. notably Gammarus duebeni, but has
emphasized [37] that a complex blend of genetic, environmental. and parasitic
factors may be responsible for biased sex ratios of this species.
The possible group selective advantage of increased R resulting from genetic
factors at the deme level (Fig. 4) is obtained without physiological cost to the
individual female, nor does it involve social mortality and hence is not altruistic.
With parasitic infections, the possibility is that the host and endoparasite have
co-evolved to produce a biased female population of the host with the same deme
adaptive advantage of increased R (Fig. 4). Both methods incur a population genetic
cost, because out-breeding is limited when fewer males are involved and also a
'founder' cost because unequal sex ratio populations are less likely to provide
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emigrant pairs able to generate new self-reproducing demes.

Photoperiod
Photoperiod was shown by Bulnheim [36] to influence the sex ratio of G. duebeni
with a preponderance of males when exposed to long days ( > 13-14 h light) and
preponderance of females on exposure to short days ( < 13-14 h light) at !5° C.
There was a critical period during ontogeny, up to the fourth molt stage. when this
response could be induced and the duration of light was the most important factor
involved. White light levels of > I lux were sufficient to produce the sex ratio
changes noted, although the wavelength of light responsible has not been determined
[37].
Photoperiod is viewed as an environmental stimulus utilized in timing the
reproductive cycle of amphipods. Sergestrale [38] discusses decreasing day lengths in
fall as a synchronizer for egg laying in the glacial relict populations of Pontoporeia
affinis in the Baltic Sea. Of two experimental populations of P. affinis kept at 3-6°C.
one in the dark and the other in continuous light, only the former had produced eggs
after 6 months. Steele et al. [39] showed that change of photoperiod was a syn-
chronizer for the single brood produced by Gammarus setosus. Thus. all short day
( < 12 h light) regimes caused accelerated sexual development, but those greater than
12 h light or in continuous darkness or in continuous light did not. These authors
[39] were able to explain why the onset of sexual activity in G. setosus was
synchronized to September over a northern range of 30° latitude because a de-
creasing 12-h photoperiod is present at both 44°N and 72°N at that time of year.
Photoperiod was shown to determine the onset and termination of sexual quiescence
in Hyalella azteca from localities at 44-50°N by DeMarch [40] although temperature
influenced the rate of the changes in the range 20-26°C. More southern populations
of Hyalella do not respond to photoperiod in this way [15]. Photoperiod must be
replaced as a synchronizer in continuously dark habitats such as the abyss, in caves,
and also in southerly locations where annual photoperiod changes become less
marked.

Other physical factors

A number of other physical factors probably influence the reproductive strategies
 13

of amphipods. Thus wind, variable by direction, speed, and timing has the effect on
water of producing waves which influence sediment stability in the littoral and near
sublittoral. Wave washout of Pontoporeia femora/a in a shallow estuary following
storms has been postulated [I 0] as the reason for the relatively high R value,
although direct evidence is not available.
Other factors depend on the habitat type occupied; for example in terrestrial and
littoral habitats, frost and ice, drought and dessication are important adaptive
considerations.

Biotic factors
Predation
The mortality pattern for the semiannual C. volutator in the Bay of Fundy (Fig. 3)
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is caused by size selection of larger individuals by their major predators, which are
migratory wading birds. Thus, the semiannual life history of C. volutator and others
shown in Table l may result from size specific mortality due to predation. Other
examples include the marine, littoral Orchestia whose chief predators are birds and
small mammals at low tide and the freshwater Gammarus and Crangonyx whose
predators are fish. Freshwater fish consume greater than 60% of the total annual
production of Gammarus pulex (41].
Nelson (42] showed, by exclusion and enclosure field experiments, that some
epifaunal amphipods are subject to greater predation pressures than infaunal
amphipods. Nelson [4] and Van Dolah and Bird [6] suggest that reproductive effort,
as measured by brood numbers, is adjusted to compensate for the increased
mortality. Nelson [4] indicates that the brood number differences result essentially
from the size differences between the two groups-the smaller sized group, inclusive
of some Ampeliscidae and Haustoridae, being infaunal and the larger size group,
including Gammaridae, being epifaunal.
The high values of R max, greater than 150, of Table I may result from an adaptive
response to predation by the prey species. This must involve predation pressure over
a considerable time period and involve co-evolution of predator and prey. Species
with R less than 150 are suggested to be adjusting R to an average of the physical
and biological factors in their environment. Predation mortality in this group is
proposed to be mediated by physical factors, such as wave-washout of Pontoporeia,
and to involve a suite of non-specific, chance predators with little co-evolution of
specific predator and prey species.

Interspecific competition
The relatively recent introduction of the cosmopolitan 0. platensis into the Baltic
Sea [43] has led to competition between this species and the endemic 0. gammarellus.
0. platensis has extended its range at the expense of 0. gammarellus which Dahl [43]
thought to be due to the superior reproductive capability of 0. platensis ( R max= 273).
Tube-living species compete for space. Nagle [44] describes aggressive interactions
between tube-living Microdeutopus damnoniensis and Corophium acutum. Infaunal
amphipods which live at certain levels within sedimentary substrates may undertake
interspecific competitive interactions as shown by Grant (45].
 14

Intraspecific competition
The experimental manipulation of density to test its effect on reproduction of the
freshwater amp hi pod, Hyalella azteca, has been studied by Wilder [ 14]. Wilder's
density experiments were run at room temperature of 16-31 oc and showed that at
high densities (up to 300 individuals per liter) there was a decrease in growth rate
and size; hence time at first oviposition was delayed. Because of dependence of
brood number on size, a decrease in the number of eggs per brood resulted. The
negative feedback controls are part of a simple social behavior homeorheostat
described in general terms for invertebrates [27]. Even at the highest densities tested
by Wilder, Hyalella could successfully produce a brood. Field observations on
H_yale/la by Strong [15] have shown that actual densities are always lower than the
carrying capacity of the environment and the density controls found in the labora-
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tory by Wilder will rarely be in operation.

Sublittoral tube building may be expected to cause space limitations at high
densities although high densities may be achieved, for example, up to 146,200
animals per m2 of Ampelisca abdita [46]. Nevertheless, intraspecific aggressive
interactions in tube builders have been recorded in Ampelisca abdita, Corophium
volutator, and Erichthonius brasiliensis [42]. It is presumably intraspecific encounters
which result in reduction of ingestion rate and hence of growth rate which cause a
negative effect on reproductive output similar to that reported by Wilder [14].

Cost of reproduction

For a given reproductive energy output, whether few. large or many, small eggs
are produced is important in determining individual or population survivorship. The
range in volume of eggs shown in Table IV. from 0.0361 to 0.2888 mm\ is an 8-fold
difference. The estimation used here is 4j3'1Tr 3 and is 13-15% higher than an
estimate based on: 4j3'1Tr 1 r 2 r 3 [47], where r 1, r2 , and r3 are half the length. breadth.
and depth of the egg in mm. respectively. Since newly laid eggs are of similar shape.
this correction has been ignored in presenting the comparative data of Table IV. The
percentage of the volume of the brood devoted to an individual egg in Table IV
ranges from 0.4 to 20%. a 50-fold difference. The smallest known egg diameter in
Amphipoda is 0.25 mm, of volume 0.0082 mm2 • from Seborgia minima [48] and each
egg volume of Table IV is expressed as a proportion of it. The largest amphipod egg
known is from Stegocephalus inflatus, an arctic species [49], with a mean diameter of
1.75 mm and volume of 2.8073 mm3, which is 342 times the Seborgia egg volume.
The adult female Seborgia is only 0.8-1.0 mm long and produces a single egg per
brood, although how many broods per female and generations per year are produced
is unknown. Proportionately more of the egg volume (as a percentage of total brood
volume, I/ b%) is devoted to the individual egg as the brood volume decreases.
confirming the importance of production of a fully formed. physiologically ad-
vanced, post-embryonic juvenile hatchling in all members of the Gammaridea so far
examined. The inverse logarithmic relationship obtained from data in Tables I to IV.
plus S. minima, is: log I jb% = 0.762-0.551 log 10 brood volume; n = 23, r = 0.86.
 Downloaded by [University of Glasgow] at 08:46 03 January 2015

TABLE IV
Estimates of egg and body volumes calculated as in Eqns. 5 and 6, respectively, based on the data in Tables 1-111

Species A B c D E F
Single egg volume Brood volume Mean body volume Reproductive cost AjC%X 10 3 Seborgia units
(mm3 ) (mm3 ) (mm3 ) (%RRJ

Orchestia cavimana 0.1721 3.10 181.53 2 10 21

0. remyi roffensis 0.1248 0.62 22.69 3 55 15
0. mediterranea 0.1955 7.04 347.04 2 6 24
Gammarus wilkitzkii 0.2038 18.34-50.95 347.13 5-12 6 25
G. setosus 0.1721 3.44-25.82 119.79 3-22 14 21
G. obtusatus 0.1439 2.45 22.69 II 63 18
G. oceanicus 0.0871 7.84 179.79 7 7 II
G. finmarchicus 0.0655 1.97 58.43 3 II 8
G. duebeni 0.0970 3.88 76.05 5 13 12
Pontoporeia femora/a 0.0477 2.27 96.90 3 5 6
Leptocheirus pinguis 0.0780 3.98 181.53 2 4 10
0. gammarellus 0.2888 5.49 254.25 2 II 35
0. platensis 0.1721-0.1076 2.41-0.43 37.45 1-6 29-46 21-13
Gammarus /awrencianus 0.0361 0.54 5.66 10 64 4
G. tigrinus 0.0510 0.56 9.78 6 52 6
G. stoerensis 0.0446 0.49 9.78 5 46 5
Hap/oops fundiensis 0.0544 0.27 15.16 2 36 7
Ampe/isca macrocepha/a 0.2682 16.09 197.19 8 14 33
Casco bige/owi 0.1727 8.60 270.27 3 6 21

Column F presents individual egg volume relative to the Seborgia egg.

V>
 16

Steele and Steele [50] have demonstrated a general relationship such that the
smaller the egg the more rapid is the ontogenetic development rate, although
amphipods and mysids showed a faster development rate at the same egg size than
other Crustacea.
For an ovigerous female, there is a physiological cost limit to brood production in
terms of the energy released in relation to the energy content of the female. That this
is the case in Amphipoda is shown by the linear, logarithmic relationship between
brood volume (Table IV) and female body length (Tables I and II) for Gammarus
and Orchestia. The fitted regression line is:
log (brood volume in mm3 X 10) = -2.53 + 1.85 log (female length in mm X 10):
n = 14, r= 0.65.
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Previous authors [2,6] have described a linear or curvilinear relationship between

body length and numbers of eggs per brood. In general, the linear relationship
pertains within a population over a narrow size range whilst the curvilinear relation-
ship applies when a wider range of sizes is sampled andjor for different populations.
The relationship between brood volume and body volume is less (Table IV) in
Orchestia (1-6%) than in Gammarus (3-22%). Individual estimates of the proportion
of body to brood volume (Table IV) suggest that there is great variation between
populations of the same species [2,3]. Thus, these data can best be used as a measure
of reproductive cost for given populations within a species.
Since body length or size in Amphipoda is primarily a function of growth rate
and generation time, both factors should be important in elucidating evolutionary
strategies of reproduction. Different growth rates result in larger or smaller body
sizes because of the relatively short ( < 3 yr) longevities so far known. The physio-
logical basis of growth and reproductive timing in Amphipoda is considered to be
regulated by an 'internal clock' consisting of an endocrine system under genetic
control and influenced by exogenous, seasonal stimuli, such as food supply, photo-
period, and temperature [51].

Discussion

The classification of amphipod life histories presented is similar to that of Morino

[3] but differs in that no distinction is made for species with a resting stage and the
categorization utilizes longevity as well as the number of broods per year. The life
history diagram is proposed as an accurate way of communicating life history data
inclusive of longevity, age at first breeding or generation time, development times of
the egg, juvenile, immature and adult, and time of brood production by specified
generations.
It is clear that life histories of Gammaridea as well as the governing mechanisms
regarding reproductive bionomics remain to be elucidated. In particular:
- the life history and reproductive potentials of Gammaridea are poorly known
from tropical, antarctic, and those species occupying habitats such as the terrestrial,
continental slope, and abyssal:
 17

- the descriptive life history and reproductive data available refer mainly to
species from the boreal regions of the continental shelf and in fresh water;
- little information is yet available regarding the genetic mechanisms involved in
sexual reproduction;
- little information is available on the energy cost of reproduction in relation to
the maintenance energy costs of the ovigerous female.
In predator-prey species pairs, such as wading birds and Corophium, the small
prey size selected for has resulted in an increase in metabolic and growth rate and a
decrease in generation time, hence many populations have a semiannual life history.
However, selection for small size in other amphipods such as Orchestia involves
decreased growth rate [ 11]. In the case of 0. remyi roffensis, growth is about 4 times
less than two other species of Orchestia which live lower on the shore [II]. The
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driving force here was suggested to be the poor nutritive value of rotting driftwood.
The slow growth resulted in small body size, small eggs and a lower R value (Tables I
and II) than in 0. gammarellus and 0. mediterranea. These reductions could be
tolerated because of the cryptozoic life style adopted by 0. remyi roffensis and the
relaxed predation pressure this must entail. These two examples show that pro-
gressive evolution may occur either by increasing or decreasing R or Rmax and brood
volume.

Acknowledgements

I would like to thank Dr. R.W. Elner, Biological Station, St. Andrews, and Dr.
D.H. Steele, Memorial University of Newfoundland, St. John's, for reading, and
improving, an earlier version of this manuscript.

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