Developmental mode in opisthobranch molluscs from the tropical eastern Pacific Ocean

2008·8.3 MB·English

by  Jeffrey H R Goddard

THE VELIGER
The Veliger 50(2):83-96 (June 20, 2008) © CMS, Inc., 2007
Developmental Mode in Opisthobranch Molluscs from the Tropical
Eastern Pacific Ocean
JEFFREY H. R. GODDARD
Marine Science Institute, University ofCalifornia, Santa Barbara, CA 93106-6150
(e-mail: [email protected])
ALICIA HERMOSILLO
Km
University ofGuadalajara, Centro Universitario de Ciencias Biologicas y Agropecuarias, 15.5 Carretera a
Nogales, Zapopan, Jalisco, Mexico
Abstract. Little has been published on mode ofdevelopment in benthic opisthobranchs from the tropical eastern
Pacific Ocean. Based on observations ofuncleaved eggs, developing embryos, or hatching larvae, we determined or
inferred mode of development for 43 species collected primarily from Bahia de Banderas, Mexico. Forty-two of
these, including the umbraculoidean Tylodinafungina, had planktotrophic development, while Phidiana lascrucensis
hatched as lecithotrophic larvae. Both the sacoglossan Elysia pusilla, which had small eggs, relatively large egg
capsules, and irregularstrandsofextra-capsularyolk in itseggmass, and the dendronotacean Lomanotus vermiformis
may also have lecithotrophic development in this region. Combined with previously existing data, mode of
development is now known for 91 species ofnative, benthic, shallow-water opisthobranchs from the eastern Pacific
and can be tentatively inferred for another 13 species based on data from other regions. Four species hatch as
lecithotrophic larvae, and the remaining 100 as planktotrophic larvae. The prevalence of planktotrophic
development in opisthobranchs from the eastern Pacific is similar to that known from the adjacent northeast
Pacific Ocean, but is higher than in the less productivewaters ofthe Caribbean Sea and the tropical western Atlantic-
Ocean, where opisthobranch eggs attain much larger diameters and 37% of the 112 species examined have either
lecithotrophic or direct development. These results agree with those known for a diverse range of marine
invertebrates across the Isthmus ofPanama and are consistent with evolutionary trends expected in the egg size and
mode ofdevelopment with historical changes in ocean productivity and larval feeding environment.
INTRODUCTION greater tropical western Atlantic Ocean (together
W
referred to hereafter as the Atlantic).
More than 90% of 126 native species ofopisthobranchs Based on the distributions reported recently by
studied from thecool temperate waters ofthe northeast Behrens & Hermosillo (2005), Camacho et al. (2005)
PacificOcean have planktotrophic development, a high and Hermosillo et al. (2006), 17 species included in
prevalence thought to reflect the region's suitability for Goddard (2004) have ranges extending well into the
larval feeding and growth, especially its generally slow Panamic province. Excepting Antaeolidiella indica
currents, large geographic expanse, and primary (Bergh 1888), which has lecithotrophic development
production driven by coastal upwelling and horizontal and is circumtropical in distribution, all have plankto-
advection via the California Current, (Goddard, 2004). trophic larval development. Gonsalves-Jackson (2001,
In contrast, relatively little information has been 2004) compared development in opisthobranchs across
published on developmental mode in opisthobranchs the Isthmus of Panama, and observed "planktonic"
from the tropical eastern Pacific (hereafter E Pacific), development in all 39 Pacific species she studied.
which includes the Panamic biogeographic province Although Gonsalves-Jackson (2004) did notdistinguish
and extends from southern Baja California Sur to between planktotrophy and pelagic lecithotrophy, the
central Peru (Briggs, 1974). Here we document small egg-sizes she reported (under 70 microns for
developmental mode in 43 species of shallow-water sacoglossans and under 115 microns for all other
opisthobranchs known from the Pacific coast of species), combined with her descriptions and illustra-
Mexico, and compare the frequencies of the major tions ofembryos and hatching larvae, reliably indicate
modes of development to those known from the NE planktotrophicdevelopment forall 39 species, based on
Pacific as well as the neighboring Caribbean Sea and morphological criteria and known egg-size distribu-
Page 84 The Veliger, Vol. 50, No. 2
J
Nayarit
*N
• * \
Punta Mita
Islas °* V \\ Mexico
Marietas Bahia de V.A
Banderas
Lindomar
^^vv* V
Los Arcos >v J
Mismaloya ~f
Pacific
Ocean
Jalisco
Figure 1. Map ofBahia de Banderas. Mexico, showing collection localities.
tions (Thompson, 1976; Bonar, 1978; Hadfield & opisthobranch Tylodinafungina Gabb, 1865. Because
Miller, 1987; Goddard, 2004). Finally, information on so little is known about the development and larvae of
the development of 13 of the more widely distributed umbraculoideans (see Gibson, 2003), we also provide
Panamic opisthobranchs has been obtained from other here a detailed description ofits egg mass and hatching
regions of the world. Owing to the possibilities of larvae.
geographic divergence and poecilogony, these latter
METHODS
data cannot be considered definitive for the E Pacific,
but do suggest that Lomanotus vermiformis Eliot 1908
Adult opisthobranchs and opisthobranch egg masses
and Phestilla lugubris (Bergh 1870) have lecithotrophic positively identified in the field were collected by hand
development, and that the remaining 11 species are from 16-28 February 2006 from subtidal and intertidal
pGoleatnzkftroiterdo,ph1i9c78(;HaSrrwiist,ze1r9-7D5u;nlBaapn,de1l9,78;197S6c;hmCelkaerlk && tsihteesswtaittehsinofBaJhaliiascdoeaBnadndNearyaasri(t2,0°o3n0'tNh,e1w0es5t30c'oWa)st,oinf
Portmann, 1982; Gonsalves-Jackson, 2004: Table 1). Mexico (Figure 1). This bay, approximately the size,
Taken together, these data suggest that the prevalence shape and depth ofMonterey Bay, California, and the
of planktotrophy in the E Pacific is similarly high to collecting localities, have been described by Hermosillo
NE
that observed in the Pacific. (2003). Local sea surface temperaturesduringourwork
To better compare developmental mode in opistho- period averaged approximately 21°C. Adults were held
branchs from the two regions, we present here data on in the field laboratory in containers (250 to 2000 ml) of
the development of45 species of opisthobranchs from seawater at 19-23°C until they laid egg masses.
the Panamic biogeographic province. We then compare Recently laid egg masses were examined using a
our results from the E Pacific to those from the more compound microscope equipped with an ocular micro-
Wseasonally stable and relatively oligotrophic waters of meter. If first cleavage had not commenced, the
Atlantic, where a shift toward larger egg sizes and diameters of a random sample of 10 zygotes were
benthic or non-planktotrophic modes of development measured in each egg mass; otherwise, an upper limit
has been documented in opisthobranch gastropods on zygote size was estimated by measuring the
(Gonsalves-Jackson, 2001, 2004), as well as other taxa, dimensions of a few randomly selected embryos at or
including bivalve molluscs, crustaceans, echinoid echi- before the gastrula stage and (or) the minimum
noderms, and bryozoans (Lessios, 1990; Jackson & dimension of tightly fitting egg capsules containing
Herrera, 1999; Marko & Moran, 2002; Wehrtmann & embryosat orbefore thegastrula stage ofdevelopment.
Albornoz, 2002; Fortunato, 2004; Moran, 2004). After initial examination, each egg mass (or a portion
During our survey, we were able observe the egg of a large egg mass) was then isolated in a separate,
masses and hatching larvae of the umbraculoidean labeled vial. The seawater in these vials was changed
)
J. H. R. Goddard & A. Hermosillo, 2007 Page 85
daily, and the egg masses examined daily for hatching. 100 um in diameter as planktotrophic, species with
Hatching larvae were then examined, measured and in eggs greater than 165 um diameter as lecithotrophic,
some cases photographed. Developmental mode and those with eggs greater than 220 um as direct
(planktotrophic, lecithotrophic and direct) and larval developers. To avoid tabulating Atlantic species more
shell type(coiledtype 1 andegg-shaped, inflated type 2) than once, we usedValdeset al. (2006) and the Sea Slug
were assigned according to the egg size distributions Forum (http://www.seaslugforum.net/) to check for
and larval morphological criteria described by Thomp- synonymies and recent taxonomic revisions.
son (1961, 1976), Bonar (1978), Clark & Jensen (1981), We used JMP (version 7.0, SAS Institute, Inc.) to (1
Hadfield & Switzer-Dunlap (1984), Hadfield & Miller conduct contingency analyses of the frequencies of
(1987) and Goddard (2004). After obtaining the above planktotrophic vs. non-planktotrophic (lecithotrophic
eggmasses, most ofthe adult specimens were relaxedin and direct) development by region, and (2) compare
7.5% MgCl2, fixed in 70% ethanol, and deposited as egg size distributions by region. For the latter we
voucher specimens in the California Academy of excluded egg size data obtained outside the regions of
Sciences. Other adults were returned alive to the field. interest, but used all other determinations of egg size
We used an underwater data logger (StowAwayTidbit, available from the above sources, even if mode of
Onset Computer Corp.) to record temperature at development is unknown. Owing to (1) the larWge
10 min. intervals in our holding containers. number of species of opisthobranchs from the
We estimated egg size for Polyceraalabe (COLLIER & Atlantic found to have non-planktotrophic develop-
FARMER 1964) and late embryo size for Lomanotus ment, and (2) the lack ofdetailed phylogenies for most
mm
vermiformis, by placing a scale bar next to egg opisthobranch taxa across the Isthmus ofPanama, we
masses in the field and taking underwater digital limited the contingency analysis of developmental
W
images. Additional data, obtained by the senior author mode by E Pacific vs. Atlantic Oceans to the
in central and southern California and Baja California, numbers offamilies, rather than species, with plankto-
(1) supplement the data for three species wecollected in trophicvs. non-planktotrophicdevelopment. To reduce
Bahia de Banderas, and (2) are given for six additional the influence of phylogenetic constraints unique to
species whose geographic ranges include the Panamic particular families, we further limited this analysis to
province. families common to both oceans.
To compare frequencies of development modes in
the E Pacific to those in the NE Pacific and the W RESULTS
Atlantic, we assigned developmental mode (according
to the criteria mentioned above) using published data We found 70 species of opisthobranchs in Bahia de
on species from the E Pacific, and then combined these Banderas and obtained data on the development of39
results with our own. We then calculated the frequen- of these. Combined with the data on six Panamic
NciEes PoafcitfhiecdbiafsfeerdenotnmGooddedsaorfdd(e2v0e04l,op2m0e0n5)t,faornd(1K)rtuhge dspeecBiaensdeorbatsa,indeadtabyonthdeesveenliooprmaeuntthowreroeutosbitdaeinoefdBfaohriaa
W
et al. (2007); and (2) the Atlantic based on data and total of 45 species (Table 1). Forty-two had plankto-
determinations of developmental mode in Bandel trophic development, and the aeolid nudibranch
(1976), Clark & Goetzfried (1978), Eyster (1980, Phidiana lascrucensis Bertsch & Ferreira 1974 had
1981), Clark & Jensen (1981), DeFreese & Clark lecithotrophic development (Table 1). Although we
(1983), Carroll & Kempf (1990), Cronin et al. (1995), obtained data on the egg and embryo size, respectively,
Ortea (2001), Gonsalves-Jackson (2004), and Pierce et of the sacoglossan Elysia pusilla (Bergh 1872) and
W
al. (2006). For 17 species from the Atlantic we dendronotacean nudibranch Lomanotus vermiformis
assigned mode ofdevelopment aseitherplanktotrophic (Table 1), we did not observe their hatching stages
or direct based on close-up images ofegg masses with and were unable to determinewith certainty theirmode
either small or large eggs/embryos in Valdes et al. of development. The former had small eggs but had
(2006); our determinations for six ofthese species were relatively voluminous egg capsules surrounded by
confirmed by information in the other references cited irregular strands of extra-capsular yolk (ECY) (Fig-
W
above for the Atlantic, giving us confidence that our ure 2). As shown by Clark & Jensen (1981), the
determinations for the other 11 species (for which no presence of these traits can indicate lecithotrophic or
other information exists) were accurate. Ortea (2001) even direct development in sacoglossans, despite
listed egg sizes for 11 Caribbean species of the otherwise small egg size. The embryos of Lomanotus
nudibranch genus Doto, but provided no information vermiformis observed in the field were large enough
on hatching stages or type of development. For six of (Table 1) that none of the three major modes of
these species we assigned developmental mode based development can be ruled out based solely on known
on the egg-size distributions known for each mode, distributions of egg size and shell size at hatching
conservatively considering species with eggs less than (Hadfield and Miller, 1987; Goddard, 2004). Clark &
i '
The Veliger, Vol. 50, No. 2
Page 86
03 >, M tU
.O ,o CU j«^.3^ U ~ a
Mf-ii nCUS"Soo°° a3 jR> *P &8 PQ 73 7033 -I 73 '=
> 77 <U O <N 03 03 3 M 22
',3"°sC•o>5O>"ismSofUtsot".a-ot5<5;u 2=2|u3 -.tu3caU-, £ac«rCCoi-UO J-It%3^6„!tCo?0i,£"o33oS3">.^&•3co-O2xd" O D.^ m0c0 'P0ShI3'Pl0£L3, pcOt--oqu ^-oo33 < 0- PL o o p0koE0p033T<J-o
o *1i) a ' ' <chu H h 7733 .9 7to3u °>u aPy a. a. a. a.
^y *3o —3a7£o3- |SOon §^r2 §2 -»a M 60
Oo3o 7oc3 +•8g>• gS-i ^o 3NKJ ^U c£CoU >w3, U"aocJu S^O.^+c_£t.l
ts *
'3o ^11 3 3 d en rn o'q*
2Ct3(uOU ,w8alU-IHc^~OCU 7»t0NM3u8 ",'*h3S3 5,Or-t. .3c£E> "3ccOuo t33c—auu ^t/J —3CS +1 p ^+1-1 +1 i+n1 <+t1 +1 +1
C3 • -E cu 2 S O t£oX
O CO t^u 9 00 <-»
i- 73 o JL, a—
3 2 ttuu cTSl (N £ U o
CO *-t CN
3
So" ^3
T
2 ~73 g g 3 To3 - ~ ^-
O S c a.
J32 I '8 | " ' S'' o t&ou c« LU
3
^£oio"S>n''2•-2SGg-d^fZJlcc>tdj%£c«<pcaggo)u..><MO°.->U,3 'u^SaM.,"§7CSc3U."^OftsO»oe o^§5!><(hui^ % Icahu 3tpo- c„*S Oo C°rD~
.IS "^&O3^^Kcg3d|1«->dO3mjS2b3a3 ScC£8rttf.''2>§5ab ^^w&;^°«g 7WMM3 3 V rrO+~~O-1 ,—oC+-311N ', 11 Vo+O1
o>C3U ^£*c"u "iSO occu;. uuH5cGtf 3"5S3o3tj t£u&CiE—O0Ji33c5u.7aSo^3 2 <^ OOcoCN/5' i0n0 a1%CO—ua3\1O V0ms—^«O0z^ V^5brO3 j«t-3du
S=3°OcP-xj m & t>u. & (Mc
~u3Ot4tsaesjU-£'oiru5urC3btus3aOuo•"m.•3tr-c-z38:uto2:_t-nsiu^^3tS> 1"cCtCy3?Cg2jOuO.s7"^-§a3rs3Ont_ g-cc>c§8uuo;..i^7CC-3(5nss_«-3OUU3b 'tCCrr3bofw-^iuOOt;je2O'- •U.Cta3OS.£&'s5O=3j£sN0(<0J2^o 0S3; .<"2 7f^ost,,,m»2uN0<0 Umbraculoidea>O^-7GfT-ivOlmg5Dogdiinnaa1C(7c0£M6A40So35I04Z cCcu1e(d85iyro9ms4geB5d)iehaa1Bp3y8uels7sri52gil'laa1C7A4S09I2ZPpioal»nsKaby•mrneymoLe1C7A40S8I5ZS9.CfcItt3u3,oa-orN0<o-r-0t>2r—"Z5an3oMtscH33hSiudae.M7-^S_ao„^r;Ka^3c=a-~uSqs^o-l"aaSmaQ>e;t?2~1Su,:s 'p"Z•0=lco—333!aa:."U.<tc|toojou OtN0<U~03P12"M^a —2m tONu0<30N
J
' 1 i
J. H. R. Goddard & A. Hermosillo, 2007 Page 87
— cd
0pcoc64qdd -"s<3a •Ecna _C>od> sccdd aPOua *CQcecQsddt 3uCod ici3dd Tamucc-3dd GscuOid cccndd ,T,oco—)sd4 •_cE3jo <.TOUs3 7uCfupac/t3jd3. ut"fn-Zj Tf—ccfinf3lddldt> •c>p-Asds TJEcDd 1cod X8ac)d Wccdu5-ddj euhg T_5n3g
0-, C3
a e 0c3d JCuO CO cd cicn oeft
cu Oh -J
uo oa c..
o > P
oa~ j.35 o o O
u ra ii a C
ttJ J3 S
—
-£ so 1^1 o
60.S V) 00 S*O o0o0 0—0 cn oOS CN
A11) —4_l t+1 oi+/-1> T+f1 Al x+T1 ^+11- c+n1 O+S1 {II
oo cd OS c~ o CN
(N CN
_ CN
A'j 0a>, h — — ri
m >,
d mo m mn OS
U cn CN
-ua H<Ei> OSI OS OS OS OS SO
XHi4)s) •o5- oOc —c w^
U
cd
A) H'I—T)
FS
w <U
O *
aWsooo3 tO+NS1 *e+n1 eVn s+d1- VSVIO SO V V V V V SOCr+-OSN<1 1 VoV+Ii1 rSC+^ON1 SOVOS Oor+S^1 OVVOi OoVS 0OV0S
OS so SO SO
o
o
c
rS-O SOOS c—On roi
OS <s> so 'w bs
OS o ~
^ 00 <u
o o
M o 3 « sOsCoS ^ I<1«) E XE PS=h3d r(jj^2u Uoo
2cd-—r ?§S1=Kao=) —rVOvN«-fii~r "0S3-Sto,is "votN*~™C~ potfa*c^ N^oO-toi r<^p*"°™S,NoOO*-sS J.&bsSJs3pN*^O—-t- <o: ^ -—Da >^3<k3«5.i o^ortN-o -—Of^St<.Nr>—o(--nT) ".«iawSsii 0oN—r*0^ Q«iH-or~" "S Os -pcn ^ s» & 2"<o =c"Si NtOsoni—f~or-."'2o^sS;a N^r-Oo*^tS
~S SUo Qacol'/^<l Q3b£eGU<O! •Q.5-^z <y: o5<tzi Xs<Suo h•2-a<UtTi tiS§C- Uc<^ •3Z3S-Q>oZ=<n^ Q Q ^s <u ^ ^S5J ri]n UOO -~. Z ^ X 2<n0CO "-5|^u
— 1
|
Page The Veliger, Vol. 50, No. 2
m
•a
o\i? :5 C £ —2 <6U0.r^l u3
1 aQc cOo couo' —o H. <JOS. U-~gr,J"|c3
<C OW -J < <f *1,
cOo OCO O
< J
-1
COO
pq
_1
«i
— c
>J) i^>
2r, _^J
co 60
O
u +c1S oc Cu>O> OC w
£
UJ
S o m m ?
_c en in v>
~ m
bt. <-> CN o—o r- ON —00 mNO
u j E NO ro 00 r*~, st
o, cd =. o+1 +1 +1 O+1 +1 +1 +1 +1
s. ^«_, <<—NN <foNi <—/") rm- NOOn C<NN mOn
-1- n —
<N
! (i)
-J (N o ^r
y:
c CO
U
X) E 1 on ON —
o
A
h o ° &
U .1
.to. oI_ -Ca3
W
e6n0 -<=U
*
g g e
u "
ON 00 fr*"-l •r*- R S
60 +' V V ' V V +1 V •S E
W60 NO
NO X O 60
c =3
'CCD o
o ^N NrO^NO |—CO si
o m C) 6
-T^fC13NO)0O oOCOCNoO .ncT-f.l 3H =G53J "C;5jO =XO3 3 U 66C>00-33goOo <2 60 co
*oS£ 053J uE 3 o 3 _3^_ C
<6C0^oo, "^~iH~1 NOriO o H OiNn © in i 25 oo NiOnO o-sf
^UN< ~-2?S NU< £5 g uN< -ss£ i<Nn 2? o r-- s: O 52,<^NI/>^lS|CcO u-, CNr/~3.^§-.^5oCtN-O~-S^ft/N0-5s T3 BO JoC3O ^a3 c^2oon- 'm--CCa3O p^co5ao
G fii ti 5; s; ^ s; to
J. H. R. Goddard & A. Hermosillo, 2007 Page 89
Figure2. Elysiapusilla. A. Detailofeggmass, showingeggcapsules(C),extra-capsularyolk(ECY),andembryos(E). B. Close-up
ofextra-capsular yolk on outside ofegg capsules.
Goetzfried (1978) reported that this species has studied, this might reduce the total number ofE Pacific
lecithotrophic development in Florida. species whose development is known, but it wouldn't
We obtained data on the development of nine significantly affect the overall prevalence (approxi-
undescribed species, eight of which are recognized mately4%) oflecithotrophic development known from
and illustrated in Behrens & Hermosillo (2005), this region. By number of species, the incidence of
Camacho et al. (2005) or Hermosillo et al. (2006), planktotrophic vs. non-planktotrophic development in
and one ofwhich (Eubranchus sp.) appears to be new. the E Pacific did not differ significantly from that
Ourrecord ofDorisimmonda (Risbec 1928) from under observed in the NE Pacific Ocean (Table 2, Likelihood
coral rubble at Punta Mita, the northern boundary of ratio r = 1-735. P = 0.188).
Bahia de Banderas, is the first sighting ofthis speciesin From the literature we were able to determine or
Mexican waters and only the second record of its infer mode ofdeveWlopment for 112 species of opistho-
occurrence outside the Indo-west Pacific (Camacho et branchs from the Atlantic (Tables 2 & 3). Lecitho-
al., 2005). Voucherspecimensforalltenofthesespecies trophic and direct modes of development were more
W
have been deposited in the California Academy of prevalent in the Atlantic compared to the E Pacific,
Sciences (Table 1). comprising 21W% and 16%, respectively, of the 112
Combined with previously existing data from the species. In the Atlantic these non-planktotrophic or
region (see Introduction), mode ofdevelopment is now non-feeding modes of development occurred in 17
known for approximately 91 species ofnative, benthic, families (Table 3) from all of the major orders and
shallow-water opisthobranchs from the E Pacific and suborders ofbenthic opisthobranchs, save the Umbra-
can be tentatively inferred for an additional 13 species culida, the development of which has not been
W
based onpublished data from other regions. The aeolid examined in the Atlantic. Sixteen of these families
nudibranchs Antaeolidiella indica and Phidiana lascru- haverepresentatives in the E Pacific, where non-feeding
censis, and likely also both the dendronotid Lomanotus development is known from four and planktotrophic
vermiformis and the aeolid Phestilla lugnbris, hatch as development from all 16 (Table 3). Limiting the
lecithotrophic larvae, and the remaining 100 as contingency analysis to these 16 families, the incidence
planktotrophic larvae (Table 2). Fifteen of the 39 E ofnon-feeding development,Wby number offamilies, is
Pacific species studied by Gonsalves-Jackson (2004) significantly higher in the Atlantic than in the E
were only identified to genus (with voucher specimens Pacific (Likelihood ratio yj = 5.830, P = 0.016).
ofeach deposited in the American Museum ofNatural The higher prevalence ofnon-planktotrophic modes
W
History). Depending on the overlap with species we ofdevelopment in the Atlantic Ocean, compared to
Page 90 The Veliger, Vol. 50, No. 2
Table 2
Number of species ofopisthobranch molluscs known or inferred to have planktotrophic, lecithotrophic or direct
development in the tropical eastern Pacific Ocean, compared to theNE Pacific and tropicalwestern Atlantic Oceans.
Mode ofdevelopment
Reaion Planktotrophic Lecithotrophic Direct Sources ofdata
NE Pacific 116 Goddard (2004, 2005) Krug et al. (2007)
E tropical Pacific 100 Harris(1975), Bandel (1976), Clark&Goetzfried (1978), Switzer-Dunlap
(1978). Schmekel & Portmann (1982), Gonsalves-Jackson (2004),
Goddard (2004), present study
W tropical 71 24 17 Bandel (1976), Clark & Goetzfried (1978), Eyster (1980. 1981), Clark &
Atlantic Jensen (1981), DeFreese & Clark (1983), Carroll & Kempf(1990),
Ortea (2001), Gonsalves-Jackson (2004). Pierce et al. (2006), Valdes et
al. 2006
Table 3
Number ofspecies ofopisthobranchs fr.om the tropical eastern Pacific and tropical western Atlantic Oceans known
or inferred to have planktotrophic or non-planktotrophic (= lecithotrophic and direct) development, by taxonomic
family. Based on sources listed in Table 2; taxonomic classification according to Behrens & Hermosillo (2005) and
Valdes et al. (2006). A blank space means that no representatives ofthat family are known from that ocean.
Tropical eastern Pacific Tropical western Atlantic
Family Planktotrophic Non-planktotrophic Planktotrophic Non-planktotrophic
Aegiretidae 1
Aeolidiidae 6 2
Aglajidae 2
Aplustndae
Aplysiidae 10 1
Arminiidae 1 1
Boselliidae
Bullidae
Caliphyllidae 1 1
Chromodorididae 9 5
Conualevidae 1
Corambidae
1
Cylichnidae 2
Dendrodorididae 3 4
Dorididae 18 4
Dotoidae 5 4
Eubranchidae 3
Facelinidae 5 3
Flabellinidae 4
Goniodorididae 2
Haminoeidae 2 1
Hancockiidae 2
Hermaeidae
Hexabranchidae
1
Limapontiidae 1 2
Lomanotidae
1 1
Oxynoidae
1 1
Placobranchidae 3 7
Pleurobranchidae 4 2
Polyceridae 4
Tergipedidae 2 1
Tritoniidae 3
Tylodinidae
1
Zephyrinidae 2
Total no. ofspecies 100 71 41
r
J. H. R. Goddard & A. Hermosillo, 2007 Page 91
uting to the evolutionary maintenance of small egg
sizes and planktotrophy in taxa not historically
constrained to non-feeding modes ofdevelopment.
A The lack ofdirectly developingopisthobranchs in the
E Pacific stands in contrast to the NE Pacific, where it
has so far been documented in 6 species (Table 2).
However, development has been examined in less than
less than half of the total number of species of
———————— opisthobranchs known from the E Pacific (see Cama-
i ' i i ' i cho et al., 2005; Hermosillo et al., 2006), and sampling
50 100 150 200 250 300 350 in the E Pacific has been biased toward outer coast
habitats and, in our study, the winter season. Addi-
tional sampling, including in estuarine habitats and
during the summer (when a different complement of
warmer water species may be present), may therefore
be needed to determine ifthe observed difference in the
frequency of this mode of development is significant.
Although direct development is not yet known for any
B opisthobranch from the E Pacific, we suspect that
Chromodoris sp. 1 of Hermosillo et al. (2006) may
hatch asjuveniles, based on its small adult size (10 mm)
and a known geographic distribution limited to the
Revillagigedo Islands, a small volcanic archipelago
located 720 km west ofmainland Mexico.
Eight ofthe species whose development weexamined
50 100 150 200 250 300 350
in this study were also identified and studied by
Egg diameter(microns) Gonsalves-Jackson (2004) in Panama. In all cases our
Figure 3. Egg size distributions, with box plots, for size measurements of eggs and embryos corresponded
Opisthobranchia from the E Pacific (n = 81 species) (A) and closely with her measurements of egg size, and our
W
the Atlantic(n = 92species)(B).Theverticallineinthebox observations and measurements of hatching larvae
plots indicates the sample median, and the diamond indicates were consistent with her sketches of embryos, only
the sample mean and 95% confidence intervals. The egg size some of which depicted embryos near hatching
distribution forthe E Pacificisbased in part on theuppersize (Gonsalves-Jackson did not provide measurements of
limits presented for some species in Table 1. The actual egg
sizes for these species are slightly smaller (see heading for shell size at hatching for any of the species she
Table 1). examined). The largest discrepancy in egg size was for
the aeolid Flabellina marcusorum. Although we record-
the E Pacific, is reflected in the strong skew toward ed its early embryos as being 73 um in largest diameter
larger egg sizes in the former (Figure 3). (indicating a slightly smaller egg diameter), and
Gonsalves-Jackson (2004) reported a mean egg diam-
DISCUSSION eter of 81.5 um, this difference is within normal intra-
specific variation, especially between different popula-
Planktotrophy isthedominantmode ofdevelopment in tions (e.g., Goddard, 1984, 2004; Todd et al., 2001).
opisthobranchs from the EPacific, asintheNE Pacific. Planktotrophy was significantly more prevalent in
W
Differences in sea surface temperatures aside, both opisthobranchs from the E Pacific than in the
regions haveproductivewaters seeminglyconducivefor Atlantic, consistent with patterns in egg size and (or)
larval feeding and growth. Seasonal, wind-induced, modeofdevelopmentdocumentedbyotherworkersfor
coastal upwelling and the slow-moving, nutrient-rich, prosobranch gastropods, bivalve molluscs, alpheid
NE
California current fuel primary production in the crustaceans, bryozoans, echinoid echinoderms and
Pacific(Bernal&McGowan, 1981; Cheltonetal., 1982; reef-forming corals across the Isthmus of Panama
Bakun, 1990; Mann & Lazier, 1991), while three types (Lessios, 1990; Jackson & Herrera, 1999; Marko &
of upwelling (wind-induced coastal, equatorial, and Moran, 2002; Wehrtmann & Albornoz, 2002; Fortu-
that associated with the cyclonic gyre known as the nato, 2004; Moran, 2004). Most of these studies
Costa Rica dome) fuels production in the E Pacific intentionallycompared lifehistorytraitsinsisterspecies
(Wyrtki, 1964; McCreary et al., 1989; Mann & Lazier, thought to have diverged as a result of the rise of the
1991; Fielder, 1992). Larval food supplies in both Isthmus of Panama, thereby ruling out phylogenetic
regions are therefore probably rarely limiting, contrib- constraints as the sole determinant of the observed
Page 92 The Veliger, Vol. 50, No. 2
geographic patterns in developmental mode. Larger 117 urn long (Table 1). Because shell type is family-
egg-sizes and non-feeding modes of development are specific (Thompson, 1976; Goddard, 2004), the state-
therefore thought to have evolved in these taxa as a ment, without measurements, by Clark & Goetzfried
result of environmental factors, namely the drop in (1976) that L. vermiformis (as L. stauberi) has an
productivityofsurfacewatersintheCaribbean Sea and inflated, type 2 shell requires confirmation, especially
W
Atlanticfollowing the rise ofthe Isthmus ofPanama given conflicting reports of shell type in the family.
(Bishop & Marra, 1984; Coates & Obando, 1996; Thompson (1961), relying on Pruvot-Fofs (1954, fig.
Collins, 1996; Allmon, 2001). In this environment, 142g) illustration of a coiled larval shell of L. genei
larger eggs (with their greater yolk reserves) might be Verany 1846 from Europe, listed this species as having
expected as one mechanism for offsetting the mortality a type 1 shell. However, Thompson & Brown (1984)
caused directly or indirectly by lower ocean productiv- characterized the family Lomanotidae as having a type
ity and a poor larval feeding environment (e.g., Vance, 2 shell, presumably based on Clark & Goetzfried's
1973; Lessios, 1990). However, evidence presented by (1976) report for L. vermiformis.
Moran (2004) for planktotrophic arcid bivalves, sug-
gests that selection forreducedegg sizes in the E Pacific Tylodinafungina Gabb 1865
(in response to increased productivity followingthe rise
of the Isthmus) may have been more important in The egg ribbons of Tylodinafungina were observed
shaping patterns ofegg size across the Isthmus in that on the surface of its yellow, keratose sponge prey,
taxon. Moran (2004) also rightly notes that differential identified in Bakus & Abbott (1980) as Aplysina
extinction ofspecieswith largeWeggs in the E Pacific and fistularis (Pallas 1766) (= Verongia thiona de Lauben-
species with small eggs in the Atlantic following the fels 1930). The egg masses were laid flat, often in
rise of the Isthmus might also be important in overlapping, convoluted layers attached primarily to
explaining recent egg size patterns. spongin fibers exposed by the grazing activity ofadults
Environmental considerations aside, phylogenetic (Figure 4A & B). The egg ribbons were similar in
constraints do not appear to be important in explaining appearance to those of T. perversa (Gmelin 1791) and
the difference in mode of development observed in T. corticalisTate 1889 known from E Australia and the
opisthobranchs across the Isthmus of Panama. Plank- Mediterranean Sea, respectively (Thompson, 1970;
totrophyisknownfromnearlyallofthe 17faWmilieswith image in Poddubetskaia, 2002). The ribbons, though
non-planktotrophic representatives in the Atlantic thin, were stiffer than those of most other opistho-
and dominates the 16 ofthose same families that also branchs (personal observations), and appeared to be
occur in the E Pacific (Table 3). Given its widespread reinforced bytransverseinternal walls(Figure 4B). Egg
distribution among evWen higher taxonomic levels of masses laid on the sponge accumulated minute, golden
opisthobranchs in the Atlantic, non-planktotrophic brown, refractile bodies 1 to 5 urn in greatest dimen-
development appears to have evolved independently in sion (Figure 4C & D, compare to 4B). These bodies
numerous lineages ofopisthobranchs in this region. were likely unicellular cyanobacteria known to be
The differences in ocean productivity and other associated with the surface layers ofspecies ofAplysina
environmental factors mentioned above apply on even (Maldonado & Young, 1998; Friedrich et al., 1999;
broadergeographicscales, and appearto be reflected in Becerro et al., 2003; Usher et al., 2004). They did not
ocean basin-wide patterns ofegg size and developmen- occur inside the egg capsules of T. fungina, and
tal mode in shallow water nudibranchs, the most appeared to accumulate in surface folds and furrows
species rich groupofopisthobranchs(Goddard 1992, in (Figure 4C & D). The refractile bodies gave the egg
preparation). In particular, data we have presented masses an opaque, pale yellow to pale orange-brown
here support the hypothesis that eastern ocean regions, appearance and were often dense enough to obscure
with their widespread upwelling, productive waters, views ofthe embryos. In 70% ethanol the egg masses,
and slow boundary currents (e.g., Mann & Lazier, like the adult slugs, turned deep purple, indicating the
1991), will tend to maintain a higher frequency of presence ofuranidine, a pigment sequestered by species
planktotrophic development compared to western of Tylodina from their sponge prey (Teeyapant et al.,
ocean regions, which have less productive waters at 1993).
mid to lower latitudes and faster boundary currents, Near hatching, the embryos fit very tightly within
which might increase the risk of advection of larvae theireggcapsules, and theeggmasses didnot appearto
away from favorable settlement sites. break down as quickly as observed in more gelatinous
opisthobranch eggmasses. Hatchinglarvaelacked both
Notes on individual species eyespots and propodium, but had a compact, lipid-rich
viscera, a distinctive, burgundy-colored mantle organ,
Lomanotus sp. 1 hatched as small, transparent, and an operculum (Figure 4E). Their type 1 shells
planktotrophic larvae with a coiled, type 1 shell averaged 126 urn in length (Table 1) and consisted of