# Comparative Reproduction Aspects of the Deep-water

Authors: K. Kapiris; M. Thessalou-Legaki
Journal: International Journal of Zoology
 (2009)

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## Abstract

In the eastern Ionian Sea, the deep-water shrimpsAristaeomorpha foliacea and Aristeus antennatus constitute a virgin fishing resource, since their maximum abundance depth exceeds commercial exploitation depths. The two sympatric species share a number of common reproductive features, such as summer reproduction. A slight temporal shift in mating activity, ovarian maturation, and spawning period was observed between species. The most notable difference was the more pronounced seasonality in reproductive activity of Aristeus antennatus compared to that of A. foliacea as evidenced by the frequency of inseminated females and functionally mature males, as well as by the shorter ovarian maturation period. Nevertheless, regarding the whole life span, both sexes of Aristeus antennatus exhibit a more extended reproductive activity in comparison to A. foliacea. No notable differentiation of both species existed in comparison to other Mediterranean regions.


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## Body

## 1. Introduction

The two red shrimps,Aristaeomorpha foliacea (Risso, 1827)
and Aristeus antennatus (Risso, 1816)
(Decapoda, Aristeidae), constitute the main target species for the demersal
deep-water fishery in the Western and Central Mediterranean, captured
exclusively by trawlers on muddy bottoms, especially near submarine trenches
and canyons. Recently, new evidence from Greek waters suggested that both resources
are adequate for exploitation at depths greater than 400 m, where at present
almost no traditional commercial trawling exists [1–3].A. foliacea is a cosmopolitan species while the geographical distributionof Aristeus antennatus is confined in the Mediterranean and the
eastern-central Atlantic. Nevertheless, Aristeus antennatus is eurybathic with a
documented depth of occurrence ranging from 80 to 3300 m ([4] and references
therein), while A. foliacea has been
recorded until now at depths from 123 to 1100 m ([5]
and references therein).
Another important feature is the longitudinal differentiation of the two
species along the Mediterranean: A.
foliacea increases in abundance from the western to the eastern Mediterranean, while the opposite is true for Aristeus antennatus.For
both species, an actual or potential commercial interest has resulted in
studies on their fisheries biology and ecology, mostly concentrated in the
western and central Mediterranean (see
references in [4, 5]).
Relatively less information exists on their reproductive
biology (e.g., [6–11]), while larval life and recruitment are still
obscure.As opposed to the western Mediterranean, the two red shrimps coexist in the eastern
Ionian both horizontally and vertically in an almost virgin condition. This was
considered as an excellent opportunity for obtaining comparable data on their
reproduction. In addition, such data, obtained for the first time for the
eastern  Mediterranean, could serve in the comparison of life history traits
along the Mediterranean.


## 2. Materials and Methods

Shrimps were collected on a monthly basis (December 1996 to November
1997) in the Greek Ionian Sea between Peloponnisos and Zakynthos Island
(depth range: 446–728 m) (Figure1), using a commercial trawl (18 mm at the cod end). In totally, 90 hauls were
carried out, in which 37301 A. foliacea specimens (17148 females, 20153 males) and 8574 A. antennatus individuals (7272 females, 1302 males) were caught. They
were sexed and measured
for carapace length (CL, mm) to the nearest 0.01 mm. The wet body weight (BW,
g) was also measured with 0.001 g accuracy.Figure 1
Map of the research area (A = deep waters of the North Ionian Sea, B = sampling area with sampling stations
(#)).Ovarian maturity stages and
spermatophore presence in the thelycum (inseminated specimens) were recorded
from fresh specimens by macroscopic observation using the empirical scales of [12]
for A. foliacea (N = 1202) and [13] for Aristeus antennatus (N = 1487). Four
stages of development were established based on the ovarian color and size:
stage I: undeveloped; stage II: developing; stage III: mature; stage IV:
spawning. In the present study, recently spent individuals (SPs) were separated
from those belonging to stage I. For the sake of comparison with other studies,
three size groups have been defined for females: CL < 30 mm (small),
30 < CL < 40 mm (medium), and CL > 40 mm (large).The gonad wet weight (GWW, g) and
the gonad dry weight (GDW, g) (the gonads were dried in a Mement Rost Frei oven
at 80° for 1 hour) were measured to the nearest 0.0001 g from 214
and 83, randomly chosen, individuals of A.
foliacea and Aristeus antennatus,
respectively. The relationship between gonad wet weight and gonad dry weight for
each species was expressed in terms of linear regressions F = a + bx, where F = dry
weight and X = wet weight, a = constant and b = slope. The difference between the dry
and wet gonad weights is the estimated water content. Gonadosomatic index (GSI)
was estimated from, randomly chosen, 502 females of A. foliacea and 384 females of Aristeus
antennatus as 100*(GWW/BW), where BW = body  weight.Data from the spawning season
(June-August) were used for the determination of CL50mf (the size at
which 50% of females have reached maturity, stage IV) by applying a typical
sigmoid symmetrical curve (logistic regression method in statgraphics 5.1 plus) P = 1/[1+e(ax+bCL)], where
P is the percentage of sexually mature individuals by size class (CL), and a, b
are constants [14]. The same equation was used for the estimation of CL50sf (size at which 50% of females bore spermatophore on their thelycum).Male maturity was checked, in a
great subsample, by the presence of the spermatophores in the terminal
ampoullae of vasa deferentia [13] in 1525 and 503 males of A. foliacea and Aristeus
antennatus, respectively. CL50sm (size at which 50% of males are
reproductive) was determined as above.Statistical differences between the
two species were tested by the nonparametric Mann-Whitney, Kruskall-Whallis,
and Kolmogorov-Smirnov tests [15]. We deemed only those independent variables
with P < .05 to be significant.


## 3. Results

### 3.1. Spermatophore Presence

Mating activity of both species, as
depicted by the frequency of females
bearing spermatophores on their thelycum (Figure2), was found to be
consistently high (>75%) for a long period (from spring to the beginning of
autumn). It seemed, however, that, although A.
foliacea’s mating activity decreased, it did not cease totally in late
autumn-early winter as in Aristeus
antennatus, and was already pronounced earlier (February). The occurrence
of the inseminated individuals among the months was not statistically different
between the two species (Kolmogorov-Smirnov, P > .05). In both species,
there was a statistically significant difference between female median CL with
and without spermatophores (Mann-Whitney test, P < .05). Thus inseminated
females were on average larger than noninseminated (CL ±SD):
mated 44.92±1.43 mm CL versus noninseminated
36.69±6.48 mm CL in A. foliacea, and inseminated 41.65±2.28 mm CL versus noninseminated 36.59±3.11 mm CL in Aristeus antennatus, in the whole study period. The smallest mated female was 25 mm and 18 mm CL, for A.
foliacea and Aristeus antennatus,
respectively.Figure 2
Monthly spermatophore occurrence inAristaeomorpha foliacea and Aristeus antennatus
females from the eastern Ionian Sea.During the study period, a size
segregation was obvious in both species regarding the start of mating after
oviposition (Table1): only the largest females were found mated just after the
reproductive season (see below) in November (A. foliacea) or January (Aristeus
antennatus), followed progressively thereafter by medium sized females. It
is worth noting that few mated small individuals (CL < 30 mm) of A. foliacea occurred only in July,
whereas those of Aristeus antennatus were present from May to October in
comparable frequencies to
other size groups. As a result,
larger females of both species exhibited a longer mating period than smaller
ones. During the reproductive period (April–September), all
females of A. foliacea sized between
34 and 53 mm CL were carrying spermatophores on their thelycum. Similarly, in
the period May–September, all Aristeus antennatus females between 37
and 55 mm CL were inseminated.Table 1
Monthly spermatophore and mature ovaries occurrence (%) per
size group forA. foliacea and Aristeus antennatus.
Presence of spermatophoreSize (mm)JFMAMJJASONDA. foliaceaCL < 30000000120000030 < CL < 40463925444850415051081044CL > 405461755652504750491910056Aristeus antennatusCL < 30003328323232030220030 < CL < 40055332935343553355200CL > 4010045334533343347352600Females with mature ovaries
(stages III and IV)A. foliaceaCL < 3000000000000030 < CL < 40000003628520000CL > 40000100100647248100000Aristeus antennatusCL < 30000000310000030 < CL < 400000484136290000CL > 40100000525933710000


### 3.2. Ovary Maturation

Although females with immature
ovaries of both aristeids were present throughout the year, all females caught
from October to March inA. foliacea and from October to April in Aristeus
antennatus exhibited immature ovaries (Figure 3). In both species, the ovarian
maturation process (appearance of stages III and IV) seemed to be rapid,
lasting one to two months. The first mature females of A. foliacea were observed (both stages III and IV = 2.6%) in spring
and summer, especially in April and peaking in June (both stages III and IV = 88%)
and decreasing progressively during the rest of summer (July, August). In Aristeus antennatus, the first females
with mature ovaries (stages III, IV) were found one month later (May, both stages
III and IV = 11.3%), increasing in June (both stages III and IV = 52%), and
reaching a maximum in July (both stages III and IV = 92%). Spent individuals
appeared in July (16%) for A. foliacea and already in June (27%) for Aristeus
antennatus. It seems, therefore, that although both sympatric species are
summer breeders, A. foliacea has a rather
earlier and more extended spawning period than Aristeus antennatus, in which reproduction processes seem to be
more accelerated.Monthly occurrence of ovarian maturity stages ofAristaeomorpha
foliacea and Aristeus antennatus females from the eastern Ionian Sea.
(a)(b)The smallest female ofA. foliacea with developed ovaries
(stage III) measured 36 mm CL and that of Aristeus
antennatus 26 mm CL.In accordance with the observation
concerning the relationship between female size and mating period, medium and
larger females of both species showed earlier ovarian maturation than smaller
ones (Table1). In spring, especially April and May, only large A. foliacea exhibited developed ovaries
(CL range: 52–66 mm), while in
summer, medium sized females entered mature condition (CL range: 32–56 mm). Finally,
at the end of the reproduction period in September, only large females were
still reproductive (CL range: 5056 mm). It is worth mentioning that smaller A. foliacea females did not contribute
to the reproductive pool. In Aristeus
antennatus, on the other hand, large- and medium-sized females showed
comparable percentages in ovary maturation during end of spring-early summer (May
and June) (CL range: 32–56 m), whereas
smaller individuals, CL range: 26–64 mm, became
mature in July. Thus A. foliacea large females have a more extended reproductive period (6 months) than medium
sized (3 months), while small ones are not reproductive. In Aristeus antennatus, on the other hand,
large and medium females with mature ovaries occur for a four-month period,
while smaller ones appear only during the peak of the reproductive season.Regarding female functional maturity
(i.e., the cooccurrence of inseminated and individuals with mature ovaries),
more than 60% of females with resting ovaries (stage I) in both species had
already mated. This percentage increased to more than 90% in females with a more
advanced ovarian stage. A considerable number of inseminated females were found
after oviposition (38% inA. foliacea and 44% in Aristeus antennatus).


### 3.3. Gonad Weight and Gonadosomatic Index

The mean gonad wet and dry weight
per maturity stage are given in Table2 for both species. There is a
statistically significant difference among the medians of both gonad weights
per stage in both aristeids (Kruskall-Wallis test, P = .011). Both gonads
weights increased from immature to mature specimens and the obtained values of
the spent individuals were between the stages I and II for both species. The
included water in the gonads decreased from the first to fourth stage due to
the yolk storage.Table 2
Mean wet gonad weight, dry gonad weight (g), water content (%
of wet gonad weight) and standard deviation (±SD) prematurity stage inA. foliacea and Aristeus antennatus females.
A. foliaceaWet weightDry weightWater contentMaturity stageMean weight ± SDMean weight ± SD% of wet weightI0.181±0.090.031±0.0177.04II0.366±0.210.074±0.0678.40III1.385±0.480.402±0.2368.57IV2.314±1.060.661±0.2465.36SP0.269±0.250.048±0.0178.45Aristeus antennatusWet weightDry weightWater contentMaturity stageMean weight ± SDMean weight ± SD% of wet weightI0.159±0.100.055±0.0473.6II0.507±0.350.150±0.0754.09III1.576±0.750.388±0.0554.25IV2.234±1.510.604±0.2459.19SP0.292±0.390.052±0.0770.91FemalesA. foliacea presented statistically higher mean values of gonad wet
weight in stages 1, IV and gonad dry weight in stages I, II, SP than those of Aristeus antennatus (Mann-Whitney test, P < .05). Females Aristeus
antennatus presented a statistically higher mean value of gonad wet weight
in stage II (Mann-Whitney test, P < .05). Almost all the values of water
content in the gonads of A. foliacea per stage were statistically significantly higher than those of Aristeus antennatus (Mann-Whitney test, P < .05). The relationship between the gonad wet weight (GWW) and gonad
dry weight (GDW) for each species was expressed by the equations (1)A.  foliaceaGDW=(GWW*0.35)−0.02,r=0.99,standard  error  ofb=0.003,Aristeus  antennatusGDW=(GWW*0.37)−0.004,r=0.97,standard  error  ofb=0.01.For both species, average GSI
increased with ovarian maturity (Table3), spent ovary GSI being between that
of stage II and I. Monthly average GSI varied seasonally (Figure 4) reaching a
maximum in summer (June, July) (7.1%) for A.
foliacea and in the same season (July, August) (7.2%) for Aristeus antennatus. The average GSI did
not statistically differ among the months between the two decapods
(Kolmogorov-Smirnov, P > .05).Table 3
Female average gonadosomatic index (±SD) ofA. foliacea and Aristeus antennatus according to the
ovarian maturity stage.
Maturity stageGonadosomatic indexA. foliaceaAristeus antennatusAverage ± SDNAverage ± SDNI0.66±0.211420.69±0.62123II1.08±0.921421.73±0.9223III6.96±2.14505.03±2.1629IV8.08±2.981247.86±2.98187SP0.91±0.78441.00±0.7822Figure 4
Temporal variation of gonadosomatic index (GSI), ofAristaeomorpha
foliacea and Aristeus antennatus from the eastern Ionian Sea.


### 3.4. Size at First Female Maturity

Based on the percentages of fully
mature ovaries and the presence of spermatophore by size class, the 50% size at
first maturity (CL50mf and CL50sf, resp.) was
determined (Table 4). In both species, CL50sf (36.84 mm CL for A. foliacea, 26.03 mm CL for A. antennatus) was lower than CL50mf,
(38.84 mm CL for A. foliacea, 29.45 mm CL for A. antennatus) indicating
that gonad maturity follows insemination. Both estimates of size at first
maturity showed that Aristeus antennatus females attain maturity at a smaller size than A. foliacea.Table 4
Elements of the logistic model (P = 1/[1+e(ax+bCL)])
for the mature (CLmf), mated (CLsf) females and mature
males (CLsm) of A. foliacea and Aristeus antennatus.
CL50aSEbSEFEMALESA. foliaceaOvarian maturity38.84 (CLmf)−10.691.380.3000.035Spermatophore occurrence36.84 (CLsf)−4.850.590.1310.013Aristeus antennatusOvarian maturity29.45 (CLmf)−5.651.650.1920.039Spermatophore occurrence26.03 (CLsf)−2.490.6060.0950.010MALESA. foliacea26.65 (CLsm)−11.662.660.680.078Aristeus antennatus19.36 (CLsm)−5.681.320.2930.053


### 3.5. Maturity of Males

The presence of the spermatophores
in the terminal ampoullae in males among the months did not differ statistically
between the two sexes (Kolmogorov-Smirnov,P > .05). Although, in A. foliacea, the occurrence of
reproductive males was consistently very high during the whole study period (87–100%), it varied
widely in Aristeus antennatus (Figure 5). In the latter species, spermatophore-bearing males existed in high
percentages before and at the beginning of female reproductive period (January
to May), while only spermatophore-deprived males existed in the middle of the
reproductive period (June), increasing thereafter until its end. In accordance
with the absence of Aristeus antennatus-inseminated
females during November and December; no male was found reproductive at that
period. The smallest reproductive male measured 26 mm and 20 mm CL, in A. foliacea and Aristeus antennatus, respectively. As in females, Aristeus antennatus males seemed to
mature at a significantly smaller size than those of A. foliacea (P = .001) (Table 4).Figure 5
Monthly occurrence of reproductive males ofAristaeomorpha
foliacea and Aristeus antennatus from the eastern Ionian Sea.


## 3.1. Spermatophore Presence

Mating activity of both species, as
depicted by the frequency of females
bearing spermatophores on their thelycum (Figure2), was found to be
consistently high (>75%) for a long period (from spring to the beginning of
autumn). It seemed, however, that, although A.
foliacea’s mating activity decreased, it did not cease totally in late
autumn-early winter as in Aristeus
antennatus, and was already pronounced earlier (February). The occurrence
of the inseminated individuals among the months was not statistically different
between the two species (Kolmogorov-Smirnov, P > .05). In both species,
there was a statistically significant difference between female median CL with
and without spermatophores (Mann-Whitney test, P < .05). Thus inseminated
females were on average larger than noninseminated (CL ±SD):
mated 44.92±1.43 mm CL versus noninseminated
36.69±6.48 mm CL in A. foliacea, and inseminated 41.65±2.28 mm CL versus noninseminated 36.59±3.11 mm CL in Aristeus antennatus, in the whole study period. The smallest mated female was 25 mm and 18 mm CL, for A.
foliacea and Aristeus antennatus,
respectively.Figure 2
Monthly spermatophore occurrence inAristaeomorpha foliacea and Aristeus antennatus
females from the eastern Ionian Sea.During the study period, a size
segregation was obvious in both species regarding the start of mating after
oviposition (Table1): only the largest females were found mated just after the
reproductive season (see below) in November (A. foliacea) or January (Aristeus
antennatus), followed progressively thereafter by medium sized females. It
is worth noting that few mated small individuals (CL < 30 mm) of A. foliacea occurred only in July,
whereas those of Aristeus antennatus were present from May to October in
comparable frequencies to
other size groups. As a result,
larger females of both species exhibited a longer mating period than smaller
ones. During the reproductive period (April–September), all
females of A. foliacea sized between
34 and 53 mm CL were carrying spermatophores on their thelycum. Similarly, in
the period May–September, all Aristeus antennatus females between 37
and 55 mm CL were inseminated.Table 1
Monthly spermatophore and mature ovaries occurrence (%) per
size group forA. foliacea and Aristeus antennatus.
Presence of spermatophoreSize (mm)JFMAMJJASONDA. foliaceaCL < 30000000120000030 < CL < 40463925444850415051081044CL > 405461755652504750491910056Aristeus antennatusCL < 30003328323232030220030 < CL < 40055332935343553355200CL > 4010045334533343347352600Females with mature ovaries
(stages III and IV)A. foliaceaCL < 3000000000000030 < CL < 40000003628520000CL > 40000100100647248100000Aristeus antennatusCL < 30000000310000030 < CL < 400000484136290000CL > 40100000525933710000


## 3.2. Ovary Maturation

Although females with immature
ovaries of both aristeids were present throughout the year, all females caught
from October to March inA. foliacea and from October to April in Aristeus
antennatus exhibited immature ovaries (Figure 3). In both species, the ovarian
maturation process (appearance of stages III and IV) seemed to be rapid,
lasting one to two months. The first mature females of A. foliacea were observed (both stages III and IV = 2.6%) in spring
and summer, especially in April and peaking in June (both stages III and IV = 88%)
and decreasing progressively during the rest of summer (July, August). In Aristeus antennatus, the first females
with mature ovaries (stages III, IV) were found one month later (May, both stages
III and IV = 11.3%), increasing in June (both stages III and IV = 52%), and
reaching a maximum in July (both stages III and IV = 92%). Spent individuals
appeared in July (16%) for A. foliacea and already in June (27%) for Aristeus
antennatus. It seems, therefore, that although both sympatric species are
summer breeders, A. foliacea has a rather
earlier and more extended spawning period than Aristeus antennatus, in which reproduction processes seem to be
more accelerated.Monthly occurrence of ovarian maturity stages ofAristaeomorpha
foliacea and Aristeus antennatus females from the eastern Ionian Sea.
(a)(b)The smallest female ofA. foliacea with developed ovaries
(stage III) measured 36 mm CL and that of Aristeus
antennatus 26 mm CL.In accordance with the observation
concerning the relationship between female size and mating period, medium and
larger females of both species showed earlier ovarian maturation than smaller
ones (Table1). In spring, especially April and May, only large A. foliacea exhibited developed ovaries
(CL range: 52–66 mm), while in
summer, medium sized females entered mature condition (CL range: 32–56 mm). Finally,
at the end of the reproduction period in September, only large females were
still reproductive (CL range: 5056 mm). It is worth mentioning that smaller A. foliacea females did not contribute
to the reproductive pool. In Aristeus
antennatus, on the other hand, large- and medium-sized females showed
comparable percentages in ovary maturation during end of spring-early summer (May
and June) (CL range: 32–56 m), whereas
smaller individuals, CL range: 26–64 mm, became
mature in July. Thus A. foliacea large females have a more extended reproductive period (6 months) than medium
sized (3 months), while small ones are not reproductive. In Aristeus antennatus, on the other hand,
large and medium females with mature ovaries occur for a four-month period,
while smaller ones appear only during the peak of the reproductive season.Regarding female functional maturity
(i.e., the cooccurrence of inseminated and individuals with mature ovaries),
more than 60% of females with resting ovaries (stage I) in both species had
already mated. This percentage increased to more than 90% in females with a more
advanced ovarian stage. A considerable number of inseminated females were found
after oviposition (38% inA. foliacea and 44% in Aristeus antennatus).


## 3.3. Gonad Weight and Gonadosomatic Index

The mean gonad wet and dry weight
per maturity stage are given in Table2 for both species. There is a
statistically significant difference among the medians of both gonad weights
per stage in both aristeids (Kruskall-Wallis test, P = .011). Both gonads
weights increased from immature to mature specimens and the obtained values of
the spent individuals were between the stages I and II for both species. The
included water in the gonads decreased from the first to fourth stage due to
the yolk storage.Table 2
Mean wet gonad weight, dry gonad weight (g), water content (%
of wet gonad weight) and standard deviation (±SD) prematurity stage inA. foliacea and Aristeus antennatus females.
A. foliaceaWet weightDry weightWater contentMaturity stageMean weight ± SDMean weight ± SD% of wet weightI0.181±0.090.031±0.0177.04II0.366±0.210.074±0.0678.40III1.385±0.480.402±0.2368.57IV2.314±1.060.661±0.2465.36SP0.269±0.250.048±0.0178.45Aristeus antennatusWet weightDry weightWater contentMaturity stageMean weight ± SDMean weight ± SD% of wet weightI0.159±0.100.055±0.0473.6II0.507±0.350.150±0.0754.09III1.576±0.750.388±0.0554.25IV2.234±1.510.604±0.2459.19SP0.292±0.390.052±0.0770.91FemalesA. foliacea presented statistically higher mean values of gonad wet
weight in stages 1, IV and gonad dry weight in stages I, II, SP than those of Aristeus antennatus (Mann-Whitney test, P < .05). Females Aristeus
antennatus presented a statistically higher mean value of gonad wet weight
in stage II (Mann-Whitney test, P < .05). Almost all the values of water
content in the gonads of A. foliacea per stage were statistically significantly higher than those of Aristeus antennatus (Mann-Whitney test, P < .05). The relationship between the gonad wet weight (GWW) and gonad
dry weight (GDW) for each species was expressed by the equations (1)A.  foliaceaGDW=(GWW*0.35)−0.02,r=0.99,standard  error  ofb=0.003,Aristeus  antennatusGDW=(GWW*0.37)−0.004,r=0.97,standard  error  ofb=0.01.For both species, average GSI
increased with ovarian maturity (Table3), spent ovary GSI being between that
of stage II and I. Monthly average GSI varied seasonally (Figure 4) reaching a
maximum in summer (June, July) (7.1%) for A.
foliacea and in the same season (July, August) (7.2%) for Aristeus antennatus. The average GSI did
not statistically differ among the months between the two decapods
(Kolmogorov-Smirnov, P > .05).Table 3
Female average gonadosomatic index (±SD) ofA. foliacea and Aristeus antennatus according to the
ovarian maturity stage.
Maturity stageGonadosomatic indexA. foliaceaAristeus antennatusAverage ± SDNAverage ± SDNI0.66±0.211420.69±0.62123II1.08±0.921421.73±0.9223III6.96±2.14505.03±2.1629IV8.08±2.981247.86±2.98187SP0.91±0.78441.00±0.7822Figure 4
Temporal variation of gonadosomatic index (GSI), ofAristaeomorpha
foliacea and Aristeus antennatus from the eastern Ionian Sea.


## 3.4. Size at First Female Maturity

Based on the percentages of fully
mature ovaries and the presence of spermatophore by size class, the 50% size at
first maturity (CL50mf and CL50sf, resp.) was
determined (Table 4). In both species, CL50sf (36.84 mm CL for A. foliacea, 26.03 mm CL for A. antennatus) was lower than CL50mf,
(38.84 mm CL for A. foliacea, 29.45 mm CL for A. antennatus) indicating
that gonad maturity follows insemination. Both estimates of size at first
maturity showed that Aristeus antennatus females attain maturity at a smaller size than A. foliacea.Table 4
Elements of the logistic model (P = 1/[1+e(ax+bCL)])
for the mature (CLmf), mated (CLsf) females and mature
males (CLsm) of A. foliacea and Aristeus antennatus.
CL50aSEbSEFEMALESA. foliaceaOvarian maturity38.84 (CLmf)−10.691.380.3000.035Spermatophore occurrence36.84 (CLsf)−4.850.590.1310.013Aristeus antennatusOvarian maturity29.45 (CLmf)−5.651.650.1920.039Spermatophore occurrence26.03 (CLsf)−2.490.6060.0950.010MALESA. foliacea26.65 (CLsm)−11.662.660.680.078Aristeus antennatus19.36 (CLsm)−5.681.320.2930.053


## 3.5. Maturity of Males

The presence of the spermatophores
in the terminal ampoullae in males among the months did not differ statistically
between the two sexes (Kolmogorov-Smirnov,P > .05). Although, in A. foliacea, the occurrence of
reproductive males was consistently very high during the whole study period (87–100%), it varied
widely in Aristeus antennatus (Figure 5). In the latter species, spermatophore-bearing males existed in high
percentages before and at the beginning of female reproductive period (January
to May), while only spermatophore-deprived males existed in the middle of the
reproductive period (June), increasing thereafter until its end. In accordance
with the absence of Aristeus antennatus-inseminated
females during November and December; no male was found reproductive at that
period. The smallest reproductive male measured 26 mm and 20 mm CL, in A. foliacea and Aristeus antennatus, respectively. As in females, Aristeus antennatus males seemed to
mature at a significantly smaller size than those of A. foliacea (P = .001) (Table 4).Figure 5
Monthly occurrence of reproductive males ofAristaeomorpha
foliacea and Aristeus antennatus from the eastern Ionian Sea.


## 4. Discussion

In the Greek Ionian Sea, fishing
pressure in depths beyond 500 m is almost absent. As a result, both aristeids
constitute an unexploited resource for this area, with a potential to support a
viable fishery [2, 3]. The unexploited status of both red shrimps is reflected in
the presence of relatively higher percentage of large shrimp in comparison to
other Mediterranean regions [16]. The relative abundance of the two species in
the study area [3] conforms to the general longitudinal differentiation of the
two species along the Mediterranean: A. foliacea shows greater abundances in
the central-eastern part, while Aristeus
antennatus in the western part.The results of the present study
demonstrated the high-reproductive capacity of both red shrimps in the study
area. A remarkable succession concerning maturing, mating, oocytes’ release of
both species, and sexes was shown. This seasonality is a common phenomenon
within the Dendrobranchiata [17]. According to
[18, 19], the most feasible pattern
of these processes during a month, at least in Aristeus antennatus, is the following: initial ovary development,
molting, mating, vitellogenesis, and spawning.Nevertheless, in the study areaA. foliacea presented weaker seasonality
in mating than Aristeus antennatus in
which a remarkable synchronism in fertilization exists as depicted by the sharp
increase of inseminated females just before and during the reproductive season.
The main mating period (>50% mated females) lasts longer in the eastern
Ionian (10 months for A. foliacea and
7 months for Aristeus antennatus)
than in Sardinian waters (8 months for A.
foliacea and 6 months for Aristeus
antennatus) [7] or the Balearic Islands (4 months for Aristeus antennatus)
[18, 19].The longer mating and reproductive period of
larger individuals in both species from the eastern Ionian has been also
pointed out from other localities (e.g.,A.
foliacea: [20] in the western Ionian Sea; Aristeus antennatus: [21, 22]). In Aristeus
antennatus, this longer period of spermatophore carrying in the thelycum
could be related to possible recoupling of these individuals during the same
reproductive period resulting in more than one spawning [18, 19]. Nevertheless,
based on the mature follicle presence and the duration of ovarian maturation, [23]
it is concluded that a single batch of oocytes should develop at each
reproductive period. It is worth mentioning that in the eastern Ionian, in spite
the fact that males in general and especially those capable of mating are
drastically decreased in the middle of the reproductive season (June to
August), spermatophore presence in females remains at the same levels. This
discrepancy can be possibly explained the ability of males to mate with
multiple females: as it is already known from studies in the western
Mediterranean, the species forms aggregations of reproductive females in a similar to the present study depth range and copulation takes place with males
represented in low percentages in the beginning of the shoal formation (see [4] for
references). Multiple spawnings could more likely occur in A. foliacea, since in the latest ovarian stage only half of the oocytes
are fully mature, the rest being in previous stages [12, 24], and, according to
the present study, mature males exist throughout the reproductive period in
high percentages.Regarding the relationship between mating and
gonad maturity, the highest proportion of the noninseminated females of both
species belonged to stage I (immature). Main mating activity precedes the
appearance of gonad maturation by four months inA. foliacea (January–April) and by
only two months in Aristeus antennatus (March-April). This
difference could be attributed to the fact that Aristeus antennatus males are mainly distributed in deeper waters
and enter the female shoal for copulation in late spring, while in the depth
range sampled, A. foliacea males and
females coexist, with sex ratio exhibiting a slight predominance of males [3].
For both species, it can be suggested that ovary development is induced by
copulation [23, 24].
Greek stock of both species seems to agree, in general, with the maturation behavior
of other Mediterranean populations: from the western Ionian Sea [20, 25, 26] and Sicily [8] for A.
foliacea, and from the Ligurian Sea [13, 21, 22], Ibiza Channel [18, 19], Portugal [25, 26], Spain
[18, 19, 23], and Algerian waters
[27] for Aristeus antennatus. Although some unessential  differences
have been reported among the several areas of the Mediterranean.Nevertheless,A. foliacea precedes Aristeus
antennatus for about a month with respect to mating, ovary maturation, and
spawning. This shift in timing of the reproductive components of the two
aristeids has been also recorded in Sicilian waters, where also the two species
coexist [7].The fully mature female minimum size
ofA. foliacea in the present study (36 mm CL) seems to be in the upper part of the range recorded from the Mediterranean
(23–40 mm CL) (see [5])
and belongs to 1+ age group, while that of Aristeus
antennatus seems to be the smallest so far recorded and belongs to 0+ age
group. Thus in the Greek Ionian Sea, Aristeus
antennatus is already sexually active from its first year of life, having a
greater ovogenetic activity than A.
foliacea. This more extensive activity of Aristeus antennatus is documented by the minimum CL for mature
individuals as well as and the smaller size at first maturity for both sexes,
in relation to A. foliacea.Reference [28] hypothesized that the
younger individuals of Aristeus
antennatus mature for the first time in June because of the puberty moult
that delays deposition time and have fewer spawnings. Since this species has an
open thelycum, mating and fertilization are completely external processes and
the spermatophore is shed off at each molting [29]. Thus at least in the larger
specimens, the processes of molting activity, the refertilization, and the multiple
spawning in the same reproductive period could be explained.Regarding GSI monthly values and prematurity
stage, the obtained values in this study were in the value range from
other studies. Thus forA. foliacea the estimated GSI values were slightly lower than those from Sicily [12] and Taiwan [24] but
higher than those from the western Ionian Sea [30].
Similarly, the GSI values for Aristeus
antennatus were higher than those from the Balearic Islands [18, 19] and
similar to those from Sicily [31] and the Catalan Sea
[18, 19]. In the present study, the two
species seem to have comparable reproductive effort, which is directed toward
fewer but larger ova in A. foliacea or numerous smaller ones in Aristeus
antennatus [11].CL50sf and CL50mf from the eastern Ionian Sea seem to be close
to the lower values reported in the literature for both species. Thus CL50sf ranges from 34 mm CL (north-eastern Tyrrhenian Sea;
[32] 0 to 46.6 mm CL (central Tyrrhenian; [33] for A. foliacea, and from 24–28 mm CL (Spanish
waters; [34]) to 28.8 mm CL (French coast; [35]) in Aristeus antennatus. Also, CL50mf ranges from 36 mm CL
(Sardinian waters; [7]) to 43 mm CL (western Ionian Sea; [20]) in A. foliacea, and from 18 mm CL
(Sardinian waters; [7]) to 35 mm CL (western Ionian Sea;
[25, 26]) in Aristeus antennatus.In the study area,A. foliacea males were ready to copulate
throughout the year, while in Aristeus
antennatus male reproductive activity was pronounced during late winter-late
spring (January-May). The fact that males of both red shrimps have a more
extensive reproductive activity than females is related to the observation that
immature females receive the spermatophores from the mature males and conserve
them till their sexual maturation. This prolonged reproductive activity of both
red shrimp males has been also reported from other authors. For Aristeus antennatus, [13, 18–20, 34]
pointed out that mature males appear all year round, but, unlike the present
results, their highest reproductive activity is observed between late
spring-late summer (from May to August). In comparison to other Mediterranean
regions, a general tendency for an earlier attainment of male maturity was
evident in the present study. The smallest mature male of A. foliacea (26 mm CL), for example, is almost the smallest ever
reported (from 25 mm CL in western
Ionian Sea [20] to 30 mm CL in Sardinia [36]), while that of Aristeus
antennatus (20 mm CL) lies toward the lower limit of the value range (15.9–26 mm CL in the
Catalan Sea) [18, 19, 25, 26]. In addition, the present value for CL50sm for Aristeus antennatus (19.36 mm CL) is
lower than any value in literature (range from 20 mm CL, Catalan Sea—Demestre,
1990—to 25 mm CL, western Ionian; [25, 26]). Like females, the males of the later
species were sexually active within the first year of their life.In conclusion, the study of the main
aspects of reproduction ofA. foliacea and Aristeus antennatus in the eastern Ionian Sea revealed that both species seem to conform to the other Mediterranean regions
with regard to their major reproductive traits (i.e., reproductive period,
presence of mature males throughout the year, and longer mating and
reproductive period in A. foliacea than in Aristeus antennatus, etc.).
The only life-history trait that seems to slightly differentiate the eastern
populations of both species is an earlier attainment of sexual maturity in both
sexes. This differentiation could be also attributed to the considerably higher water
temperature in the eastern Ionian Sea than in
the western most areas [37]. Nevertheless, in order to arrive to secure
conclusions, our knowledge on the eastern Mediterranean deep-sea shrimp has to
be improved by further studies on these populations and also by including a
broader ecosystem approach.



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*Source: 979512-2008-11-04.xml*