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Swimming crab Charybdis smithii of the Indian Ocean: key link in the pelagic trophic web

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crabs of thePortunidaefamily arediverse (>200species inthe Indo-Pacific), abundantcrustaceans inhabitingshallow-water benthicenvironment, continentalslope and deepwaterseamounts. Larvaeof Portunids are commonin the tropical zooplankton.Benthic adults are able toswim in the water columnusing natatory legs,but cannot residein the pelagic zone.Indian Ocean swimmingcrab Charybdis smithiiextends its distributionfar offshore and becomestruly pelagic at past-larvaephase of life.We present analysis of datacollected by YugNIRO(Ukraine) and IRD (France)from 1961 to 2005.We combine these dataseries and two samplingmethods (towed gears andstomachs of the pelagic toppredators) to present newinformation on the biologyof this species.
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BY EVGENY ROMANOV 1 FRÉDÉRIC MÉNARD 1 ,MICHEL POTIER 2 AND VENIAMIN ZAMOROV 3 EMAIL:[email protected] CONCLUSION. Although pelagic phase of life is typical for marine benthic crustaceans, extended pelagic dispersal on post-larval stages is rare phenomenon known only for highly productive upwelling areas where high production support survival and growth of juvenile-adult individuals. The Indian Ocean monsoon system and oceanic circulation likely facilitates transport of adult crabs inshore for physiological maturation and reproduction, allowing to maintain expanded and stable population despite strong natural mortality in pelagic waters due to predation. Our data evidences that swimming crabs play an important role (both as prey and predator) in the oceanic ecosystem. These results emphasize usefulness of marine predators to gain valuable information on the biology of poorly know species of the intermediate trophic levels. Swimming crabs of the Portunidae family are diverse (>200 species in the Indo-Pacific), abundant crustaceans inhabiting shallow-water benthic environment, continental slope and deepwater seamounts. Larvae of Portunids are common in the tropical zooplankton. Benthic adults are able to swim in the water column using natatory legs, but cannot reside in the pelagic zone. Indian Ocean swimming crab Charybdis smithii extends its distribution far offshore and becomes truly pelagic at past-larvae phase of life. We present analysis of data collected by YugNIRO (Ukraine) and IRD (France) from 1961 to 2005. We combine these data series and two sampling methods (towed gears and stomachs of the pelagic top predators) to present new information on the biology of this species. Published pelagic records (a) are associated with coastal waters off East Africa, Arabian Peninsula and both coasts of Hindustan. Benthic records extend as far as Madagascar, Natal and Cape Town. Our data (b) clearly demonstrate that this crab spreads over the pelagic zone of the western equatorial Indian Ocean. 1 IRD, UR 109 Thetis, Centre de Recherche Halieutique, avenue Jean Monnet BP 171, 34203 Sète, France 2 IRD, BP 172, 97492 Ste Clotilde Cedex, La Réunion, France 3 I. I. Mechnikov Odessa National University (ONU). 2, Dvoryanskaya St., 65000, Odessa, Ukraine Design and layout: IRD-CRH, 2007 Swimming crab Charybdis smithii of the Indian Ocean: key link in the pelagic trophic web Carapace width (CW) of crabs of the pelagic zone ranged with- in 23-70 mm (mean 45.1 ± 7.1 mm) and our biggest crabs reached the maximum size recorded from the benthic popula- tions. YFT, BET, LAX and trawls sampled crabs of the same size range. Crabs are favourable prey for predators due to small size, poor avoidance behaviour and post-capture handling (easy to swallow). Swimming crabs density in the aggregations is low: ~ 0.156 ind. m -3 (van Couwelaar et al. 1997). These spatial distribution features could explain very rare crab occurrence in the stomachs of surface tunas, which usually target compact schools of prey. Two moults could be associated with allometric changes: one pre-puberty moult (33-36 mm CW) and moult to morphomet- ric maturity at 45-55 mm CW. Same maturity size was observed in the benthic populations off India (Balasubrama- nian Suseelan, 1998). No physiologically mature crabs were found in the pelagic waters, suggesting that C. smithii reproduction linked with a benthic phase of life. Successful aquarial breeding of the surface caught crabs (B. Meyer, pers. comm.) proves that crabs reach maturity after set- tlement. Photo of Charybdis smithii from Türkay and Spiridonov. 2006, is presented here with permission of the authors. Photo of Carcharinus falciformis: Myers, P., R. Espinosa, C. S. Parr, T. Jones, G. S. Hammond, and T. A.Dewey. 2006. The Animal Diversity Web. Natosquilla inve s t i g a- toris exhibits same life pattern as swimming crab: benthic reproduc- tion, pelagic larvae, growth to definitive size but no maturation in pelagic zone. Long-term data demonstrates that swimming crabs occurred regularly in the pelagic waters. Its pelagic abundance usually decreased during outbursts of stomatopod Natosquilla inve s t i g a t o r i s, which dominated pelagic crustacean communities in 1965-67, 1971-74, and 2000-05 (Losse Merrit, 1971, Demidov, 1972, Potier et al., 2007). Stomatopod predation on crab pelagic larvae could explain this interaction. A mechanism of sudden stomatopod outbursts is another unsolved question for the western Indian Ocean. First cohorts appeared in the pelagic zone in June-July with onset of SW monsoon. Since development of tropical Portunid from hatching to first post-larvae instar lasts approx. 25-35 days, spawning take place during April-May – before onset of the monsoon upwelling. Seasonal abundance trend and monthly size variations sug- gest a 1-year life cycle. Rare occurrence of single big individu- als throughout the year could be attributed to high variability in the growth rate or to the survival of crabs one year after. Crabs occurred in the stomachs all year round with a maxi- mum at the end of South-western monsoon and during the autumn inter-monsoon (August-November). They almost disappear in March-April (spring inter-monsoon) due to predation, natural mortality (Christiansen Boetius, 2000) and settlement for maturation and reproduction. Indian Ocean swimming crab No pelagic reproduction Circular transport by oceanic gyres High probability of return inshore for settlement and benthic reproduction. Circular gene flow within monsoon gyre systems High trophic level on post larvae stages, low trophic level of larvae Growth to definitive size in pelagic zone Low packing density of pelagic swarms Prey of subsurface predators (long-line caught fish) Eastern Pacific red crab Both benthic and pelagic reproduction Oceanic populations depend on offshore transport Low probability of backward recruitment of parent stock from pelagic spawning Low trophic level at all pelagic stages Growth to definitive size in pelagic zone High density of pelagic swarms Prey of the surface predators (bait-boat and purse seine caught fish) Charybdis smithii vs. Pleuroncodes planipes Eastern Pacific Ocean gives an example of similar phenomena among two species: red galatheid crab Pleuroncodes planipes and swimming crab Euphylax dovii. Although both species was recorded as far as 1000 miles offshore, their distribu- tion is closely related with productive coastal upwelling areas (Alverson 1963, Jerde 1967, Longhurst 2004). For yellowfin tuna (YFT) and lancetfish (LAX), swimming crabs are dominant prey (up to 95 % of the Index of Relative Importance - IRI). For big- eye tuna (BET), crab is an important secondary prey. Annual consumption of crabs by tuna was esti- mated to 10 0 00000 t from a bioenergetic approach (Romanov Zamorov 1999). Thus crab should be one of the most abundant species of the intermediate trophic level. Crabs prey on fishes, crustaceans and squids and represents therefore an important link in the trophic pathways of the pelagic food web. More than 30 species of pelagic predators preyed on swimming crab including yellowfin tuna (Thunnus albacares), bigeye tuna (T. obesus), blue shark (Prionace glauca), silky shark (Carcharhinus falciformis), longnose lancetfish (Alepisaurus ferox), dolphinfish (Coryphaena hippurus) and pelagic stingray (Pteroplatytrygon violacea). Fishes feeding on crab are usually caught in the subsurface layers (50-350 m) by longlines. Al- though abundant swarms of crabs were observed at the sea surface, they are rare in the stomachs of surface fish caught by purse seines. a b
Transcript

BY EVGENY ROMANOV1

FRÉDÉRIC MÉNARD1, MICHEL POTIER2 AND VENIAMIN ZAMOROV3

EMAIL:[email protected]

CONCLUSION. Although pelagic phase of life is typical for marine benthic crustaceans, extended pelagic dispersal onpost-larval stages is rare phenomenon known only for highly productive upwelling areas where high production supportsurvival and growth of juvenile-adult individuals.The Indian Ocean monsoon system and oceanic circulation likely facilitates transport of adult crabs inshore forphysiological maturation and reproduction, allowing to maintain expanded and stable population despite strong naturalmortality in pelagic waters due to predation.Our data evidences that swimming crabs play an important role (both as prey and predator) in the oceanic ecosystem.These results emphasize usefulness of marine predators to gain valuable information on the biology of poorly knowspecies of the intermediate trophic levels.

Swimmingcrabs of thePortunidaefamily arediverse (>200species in

the Indo-Pacific), abundantcrustaceans inhabitingshallow-water benthicenvironment, continentalslope and deepwaterseamounts. Larvaeof Portunids are common in the tropical zooplankton.Benthic adults are able toswim in the water columnusing natatory legs,but cannot reside in the pelagic zone.Indian Ocean swimmingcrab Charybdis smithiiextends its distribution far offshore and becomestruly pelagic at past-larvaephase of life.We present analysis of datacollected by YugNIRO(Ukraine) and IRD (France)from 1961 to 2005.We combine these dataseries and two samplingmethods (towed gears andstomachs of the pelagic toppredators) to present newinformation on the biologyof this species.

Published pelagic re c o rds (a) are associated with coastal wa t e rs off EastA f r i c a , A rabian Peninsula and both coasts of Hindustan. Benthic re c o rd sextend as far as Madagascar, Natal and Cape To w n .Our data (b) clearly demonstrate that this crab spreads over the pelagic zoneof the western equatorial Indian Ocean.

1 IRD, UR 109 Thetis,Centre de Recherche Halieutique,avenue Jean Monnet BP 171, 34203 Sète, France

2 IRD, BP 172, 97492 Ste Clotilde Cedex, La Réunion, France

3 I. I. Mechnikov Odessa NationalUniversity (ONU). 2, Dvoryanskaya St.,65000, Odessa, Ukraine

Design and layout: IRD-CRH, 2007

Swimming crab Charybdis smithiiof the Indian Ocean:key link in the pelagic trophic web

C a rapace width (CW) of crabs of the pelagic zone ranged with-in 23-70 mm (mean 45.1 ± 7.1 mm) and our biggest cra b sre a ched the maximum size re c o rded from the benthic popula-t i o n s.

Y F T, B E T, LAX and trawls sampled crabs of the same size ra n g e.

C rabs are favo u rable prey for pre d a t o rs due to small size, p o o ravoidance behaviour and post-capture handling (easy to swa l l o w ) .Swimming crabs density in the aggregations is low: ~ 0.156 ind. m- 3

( van Couwelaar et al. 1 9 9 7 ) . These spatial distribution feature scould explain ve ry ra re crab occurrence in the stomachs of surfa c et u n a s, wh i ch usually target compact schools of prey.

Two moults could be associated with allometric changes: onep re-puberty moult (33-36 mm CW) and moult to morphomet-ric maturity at 45-55 mm CW. Same maturity size wa so b s e r ved in the benthic populations off India (Balasubra m a-nian Suseelan, 1 9 9 8 ) .No physiologically mature crabs were found in the pelagicwa t e rs, suggesting that C. smithii re p roduction linked with abenthic phase of life.Successful aquarial breeding of the surface caught crabs (B.M eye r, p e rs. comm.) pro ves that crabs re a ch maturity after set-t l e m e n t .

Photo of Charybdis smithii from T ü rk ayand Spiridonov. 2 0 0 6 , is presented herewith permission of the authors.

Photo of Carcharinus falciformis:Myers, P., R. Espinosa, C. S. Parr,T. Jones, G. S. Hammond,and T. A.Dewey. 2006.The Animal Diversity Web.

Natosquilla inve s t i g a-toris exhibits same lifepattern as swimmingc rab: benthic re p ro d u c-t i o n , pelagic larva e,g rowth to definitive sizebut no maturation inpelagic zone.

Long-term data demonstrates that swimming crabs occurre dregularly in the pelagic wa t e rs.Its pelagic abundance usually decreased during outbursts ofstomatopod Natosquilla inve s t i g a t o r i s, wh i ch dominatedpelagic crustacean communities in 1965-67, 1 9 7 1 - 7 4 , a n d2000-05 (Losse Merrit, 1 9 7 1 , D e m i d o v, 1 9 7 2 , Potier et al.,2 0 0 7 ) .Stomatopod predation on crab pelagic larvae could explain thisi n t e ra c t i o n .A mechanism of sudden stomatopod outbursts is anotheru n s o l ved question for the western Indian Ocean.

Fi rst cohorts appeared in the pelagic zone in Ju n e - July withonset of SW monsoon. Since development of tropical Po r t u n i df rom hatching to first post-larvae instar lasts appro x . 2 5 - 3 5d ay s, s p awning take place during Ap r i l - M ay – befo re onset ofthe monsoon upwelling.Seasonal abundance trend and monthly size variations sug-gest a 1-year life cy c l e. R a re occurrence of single big individu-als throughout the year could be attributed to high va r i a b i l i t yin the growth rate or to the survival of crabs one year after.

C rabs occurred in the stomachs all year round with a maxi-mum at the end of South-western monsoon and during theautumn inter-monsoon (Au g u s t - N o ve m b e r ) .Th ey almost disappear in March - April (spring inter- m o n s o o n )due to pre d a t i o n , n a t u ral mortality (Christiansen Boetius,2000) and settlement for maturation and re p ro d u c t i o n .

Indian Ocean swimming crab

No pelagic repro d u c t i o n

Circular transport by oceanicg y r e s

High pro b ability of returninshore for settlement and benthic repro d u c t i o n .Circular gene flow withinmonsoon gyre systems

High trophic level on post larva es t ag e s , l ow trophic level of larva e

G rowth to definitive size in pelagic zone

L ow packing density of pelag i cswa r m s

P r ey of subsurface predat o r s(long-line caught fish)

Eastern Pacific red crab

Both benthic and pelag i cr e p ro d u c t i o n

Oceanic populations depend onoffshore tra n s p o r t

L ow pro b ability of back wa r drecruitment of parent stockf rom pelagic spaw n i n g

L ow trophic level at all pelag i cs t ag e s

G rowth to definitive size in pelagic zone

High density of pelagic swa r m s

P r ey of the surface predat o r s( b a i t - b o at and purse seinecaught fish)

C h a rybdis smithii vs. P l e u roncodes planipesEastern Pacific Ocean gives an example of similar phenomena among two species:red galatheid crab Pleuroncodes planipes and swimming crab Euphylax dovii.Although both species was re c o rded as far as 1000 miles offshore, their distribu-tion is closely related with pro d u c t i ve coastal upwelling areas (Alve rson 1963,Je rde 1967, L o n g h u rst 2004).

For yellowfin tuna (YFT) and lancetfish (LAX),swimming crabs are dominant prey (up to 95 %of the Index of Relative Importance - IRI). For big-eye tuna (BET), c rab is an important secondaryp rey.Annual consumption of crabs by tuna was esti-mated to 10 0 00000 t from a bioenerg e t i ca p p ro a ch (Romanov Zamorov 1999). Thus cra bshould be one of the most abundant species ofthe intermediate trophic leve l .C rabs prey on fishes, crustaceans and squidsand re p resents there fo re an important link in thet rophic pathways of the pelagic food web.

M o re than 30 species of pelagic pre d a t o rs preye don swimming crab including yellowfin tuna( Thunnus albacare s ) , b i g eye tuna (T. o b e s u s ) , b l u es h a rk (Prionace glauca), s i l ky shark (Carch a r h i n u sfa l c i fo r m i s ) , longnose lancetfish (Alepisaurusf e ro x ) , dolphinfish (Coryphaena hippurus) andpelagic stingray (Ptero p l a t y t rygon violacea).Fishes feeding on crab are usually caught in thes u b s u r face laye rs (50-350 m) by longlines. A l-though abundant swarms of crabs were observe dat the sea surfa c e, t h ey are ra re in the stomachs ofs u r face fish caught by purse seines.

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