Reproduction in two sympatric Iberian nudibranch species (Gastropoda: Opisthobranchia) with contrasting development types

2012·6.3 MB·English

by  Goncalo Calado

© Sociedad Española de Malaeología Iberus, 30 (1): 103-110, 2012
Reproduction in two sympatric Iberian nudibranch species
(Gastropoda: Opisthobranchia) with contrasting develop-
ment types
Reproducción en dos especies simpátricas de nudibranquios
(Gastropoda: Opisthobranchia) de la Península Ibérica con tipos de
desarrollo alternativos
Gonzalo CALADO*, Cláudia SOARES** and Ricardo C. NEVES***
Recibido el 16-XI-2011. Aceptado el 7-X1I-2011
ABSTRACT
Doriopsillo areolato and D. pelseneeri are two sympatric species from the Iberian Penin-
sula that contrast in their reproductiva modes. In this study we investigated the develop-
mental mode of both species, comparing egg number and egg volume. In addition, we
investígate whether the type of development influences the amount of energy allocated for
reproduction.
Animal weight was found to be positively correlated with egg number per egg mass but not
with egg volume, which seems to be a specific character in both species. Moreover, our results
suggest that both species allocate the same amount of energy for reproduction, in terms of
body weight, though a clear difference in the way these resources are used was actually
observed. Doriopsillo areolato invested 2.22 ± 1.87% of body weight (n=3ó) essentially for
egg production, whereas D. pelseneeri invested 5.72 ± 3.31% of body weight (n-l 1) on
rich gel matrix spawn masses. The different type of development could provide an explana¬
ron for the difference in the geographical range of both species, but further studies are required.
RESUMEN
Doriopsillo areolato y D. pelseneeri son dos especies simpátricas en la Península Ibérica,
que contrastan en sus modos de reproducción. En este trabajo se investigó el modo de
desarrollo de ambas especies, comparando el número y el volumen de huevos. Además,
se investiga si el tipo de desarrollo influye en la cantidad de energía dedicada a la repro¬
ducción.
El peso del animal muestra una correlación positiva con el número de huevos por masa
de huevos, pero no con el volumen del huevo, que parece ser un carácter específico en
ambas especies. Nuestros resultados sugieren que ambas especies asignan, en términos
de peso corporal, la misma cantidad de energía para la reproducción, pero la forma en
que estos recursos se utilizan es diferente. Doriopsillo areolato, invirtió 2,22 ± 1,87% de
su peso corporal ¡n = 36), esencialmente para la producción de huevos, mientras que D.
pelseneeri ha invertido 5,72 ± 3,31% de su peso corporal (n = 1 1) en la matriz de gel
enriquecido de las masas. El tipo de desarrollo podría explicar la diferencia en la distribu¬
ción geográfica de las dos especies, pero se necesitan más estudios.
Universidade Lusófona de Humanidades e Tecnologías, Av. do Campo Grande, 376, 1749 - 024 Lisboa,
Portugal (e-mail: [email protected])
** Centro de Ciencias do Mar Universidade do Algarve, Campus de Gambelas 8005-139 Faro, Portugal
*** Biozentrum, University of Basel, Klingelbergstrasse 50, CH-4056 Basel, Switzerland
103
Iberus, 30 (1), 2012
INTRODUCTION MATERIALS AND METHODS
As far as their reproduction is con¬ Animáis of both species were col-
cerned, opisthobranchs display a diver- lected from two localities along the
sity of strategies (Rudman and Willan, Arrabida coast (West Portuguese Coast)
1998). Several works report on species and Ria de Ferrol (Galicia, NW Spain).
displaying difieren! larval development The exact localities can be found in
types: planktotrophy, lecithotrophy, and So ARES AND CALADO (2006). All speci-
direct development (Hadfield and mens were collected by hand while
Switzer-Dunlap, 1984; Hadfield and scuba diving at 5-15 m depth from
Miller, 1987; Bouchet, 1989; Todd, March to July of 2003, in the period
1983). However, the selective factors in reported as the peak of their reproduc¬
determining these larval strategies tion period.
remain to be ascertained. According to Animáis were maintained under lab-
Hadfield and Miller (1987), for any of oratory conditions as described else-
those three "different means to the same where (Soares and Calado, 2006).
end" the time required to reach the juve- Specimens were paired periodically for
nile stage is variable; usually, the larger copulation and after approximately one
the egg, the longer the pre-hatching week, egg masses were laid and
period. removed immediately. In order to estí¬
Doriopsilla areolata (Bergh, 1880) and mate the number of eggs, spawn masses
Doriopsilla pelseneeri (d'Oliveira, 1895) were measured (top, base length, and
are two radula-less, porostomate nudi- width). We collected a total number of
branchs belonging to the family 61 Doriopsilla areolata and 39 D. pelse¬
Dendrodorididae. They are amongst neeri, from which we studied 43 and 21
the most common nudibranchs inhab- laid egg masses, respectively. Each set
iting the Iberian coasts. Although animal-spawn mass was weighed in
sympatric and occasionally feeding fresh for later use in calculations.
upon the same sponges (GC, personal As for Doriopsilla areolata, three Imm
observations), both species have rather wide transverse sections of the egg
different types of development. Doriop¬ masses were cut for observation under a
silla areolata has a planktotrophic stereomicroscope. Spawns from D. pelse¬
development type, producing egg neeri were observed intact under a stere¬
masses that are formed by numerous omicroscope. Immediately after oviposi-
small eggs, while D. pelseneeri displays tion, and before any cleavage was
a metamorphic, direct development observed, eggs were counted in a
type and produces a lower number of known egg mass area and its larger
larger eggs (Soares and Calado, diameter measured to estímate egg
2006). number per egg mass and egg volume,
The known geographical range is respectively.
also different. Doriopsilla areolata is In order to establish a calibration
known to occur between the North coast curve fresh weight/dry weight, three
of Spain and the Cape Verde Islands Doriopsilla pelseneeri specimens and four
(including the Mediterranean Sea), D. areolata specimens were weighed
Ghana and Angola, whereas D. pelse¬ without water excess and dried at 60°C
neeri is restricted to the Atlantic and to constan! weight (Smith and Sebens,
Mediterranean coasts of the Iberian 1983). Afterwards, a fraction of all dried
Peninsula. The aim of this study is to samples were used to calcúlate ash
compare the developmental mode of valúes by ignition (3 hours at 550°C in a
both species, comparing egg number muffle furnace), by the estimation of
and egg volume. Further, we intend to ash-free dry weight equivalents
test whether the type of development (Havenhand and Todd, 1988; Todd,
influences the amount of energy allo- 1979). The same procedure was used on
cated for reproduction. five egg masses of each species, as well
104
Calado ETal.: Reproduction in two sympatric Iberian nudibranch species
D. pekeneeri adult weigrh (g)
Figure 1. Relationship between egg number per egg mass and adult animal weight for (A) D. areo-
lata (R2= 0.563) and (B) D. pelseneeri (R2= 0.768).
Figura 1. Relación entre el número de huevos por masa de huevo y peso del animal adulto en (A) D.
areolatá (R2- 0,563) y (B) D. pelseneeri (R2= 0,768).
as in two spawn masses of D. pelseneeri, between egg masses of the distinct pop-
from which eggs were previously ulations (Portugal and Spain) were also
removed manually. For D. areolata it was investiga ted.
assumed that egg masses were entirely
composed of eggs, since it was impossi-
ble to detach eggs from the feeble gel RESULTS
matrix. A measure of the reproductive
effort per egg mass was calculated as Egg number per egg mass and egg
the ratio between the dry weight of a volume
single egg mass and the dry weight of As presented in Soares and
the progenitor adult inferred from the Calado (2006), the egg number per egg
fresh weight by the calibration curve. mass in D. areolata was estimated to be
Finally, how much energy (inferred by between 5,500 - 240,000 eggs (n-43),
the amount of biomass) is allocated per whereas in D. pelseneeri egg number
egg mass and per egg unit, was calcu¬ varied from 300 to 5,000 (n=15) eggs per
lated. egg mass.
Statistical analyses were conducted In both species it is clear that egg
using STATISTICA (Release 6.0). Regres- number in a single spawn mass is posi-
sion analysis was performed to investí¬ tively correlated with animal weight
gate the relationship between both egg (R2= 0.563 for Doriopsilla areolata and
number and egg volume (mean valúes) R2= 0.768 for D. pelseneeri) as can be
and adult body weight. Differences seen in Figure 1. The geographical area
105
Iberus, 30 (1), 2012
D. areolata adult weigrh (g)
Figure 2. Relationship between egg volume and adult animal weight for (A) D. areolata (R2=
0.006) and (B) D. pelseneeri (R2= 0,240).
Figura 2. Relación entre el volumen del huevo y peso del animal adulto en (A) D, areolata (R2= 0,006)
y (B) D. pelseneeri (R2= 0,240).
from where animáis were collected whereas D. areolata contains 84.20 ±
seems to have no influence on this 2.41% (n=4), which reveáis a similar
analysis. However, specimens from hydrate condition in both species. From
Galicia were observed to be slightly the ash content analysis it was estimated
smaller and therefore to deposit smaller that D. pelseneeri contains 4.30 ± 1.42%
egg masses than those collected in Por¬ (n=3) of inorganic matter in the body,
tugal. whereas D. areolata contains 7.95 ±
Moreover, it was observed that egg 1.34% (n:=4) (mean valúes).
volume does not appear to co-vary with Doriopsilla pelseneeri egg masses con-
animal weight (R2= 0.006 for Doriopsilla tained 90.57 ± 3.03% (n=5) of water and
areolata and R2= 0.240 for D. pelseneeri) 4.13 ± 0.89% (n=5) of inorganic matter,
as illustrated in Figure 2. Indeed, egg whereas D. areolata egg masses con-
volume seems to be a specific character tained 92.73 ± 2.08% (n“5) of water and
in both species. 4.55 ± 0.85% (n=2) of inorganic matter
(mean valúes). In the former species egg
Reproductive investment in the masses are made of 39% of eggs and
two species 61% of gel matrix, which contains 88.53
Dry weight analysis revealed that ± 1.66% (n=2) of water and 6.90 ± 1.08%
Doriopsilla pelseneeri's body contains on (n~2) of inorganic matter. Since for D.
average 87.94 ± 2.22% (n=3) of water. areolata it has been impossible to detach
106
Calado ETal.: Reproduction in two sympatric Iberian nudibranch species
Weight % invested
per egg (xlO'^)
0 1 3 4 5 6 7 9 10 11 12 13 14 20 21 22 23 24 25
B
D. aerolata
D. pebeneeri
Weight % invested
per egg masse
-j^^-1
0 1 2 3 4 5 6 7 8 9 10
Figure 3. Relationship between weight invested (A) per egg mass and (B) per egg (%) for D. areo-
íata and D. pelseneeri.
Figura 3. Relación entre el peso invertido (A) por unidad de masa de huevos y (B) por huevo (%) para
D. areolataj D. pelseneeri.
eggs from the jelly matrix, egg masses D. areolata, invested 2.22 ± 1.87% (n=36,
were assumed to be made up nearly mean valué of the range 0.012% -
100% of eggs. 4.767%) (Fig. 3B).
With these valúes we obtain that D.
pelseneeri invested 0.0012 ± 0.0009% of
their weight per single egg (n^ll, mean DISCUSSION
valué of the range 0.00009% - 0.00243%),
while D. areolata invested 0.00026 ± Developmental patterns in opistho-
0.00009% of their body weight per branchs have been a subject of much
single egg (n-36, mean valué of the Ínteres! in the last decades (e.g. Had-
range 0.0000032% ^ 0.00039%) (Figure FIELD AND SWITZER-DUNLAP, 1984; FIaD-
3A). The investment per egg mass was EIELD AND MlLLER, 1987; TODD, 2001,
also calculated; Doríopsilla pelseneeri Krug, 2009). However, obtaining a final
specimens studied invested 5.72 ± 3.31% consensus has not been possible so far
of their body weight (n=ll, mean valué and some authors claim that there is no
of the range 0.305% - 9.479%), whereas single answer to what determines the
107
Iberus, 30 (1), 2012
developmental mode of any individual specific regardless of the geographic area,
opisthobranch species (Hadfield and and henee of the population.
Miller, 1987). Although sympatric and As Strathmann (1986) refers, "dif-
feeding on the same food Ítems, Doriop- ferences in size and body plan account
silla pelseneeri and D. areolata exhibit dif- for much of the variation in types of
ferent developmental patterns. Soares larval deveiopment". Recently and
AND Calado (2006) demonstrated that using opisthobranchs as a model,
D. areolata with planktotrophic develop“ Goddard (2004) agrees with this point
ment takes approximately half the time of view. This author argües that phylo-
till hatching than D. pelseneeri with genetic constraints on developmental
direct deveiopment. mode can be severe. For instance, if a
Even with rather opposite develop¬ feeding structure is lost the possibility
mental modes both species allocate of it being regained is very remóte, con-
about the same amount of energy for straining the whole lineage to a non-
reproduction, as inferred from differ- feeding developmental mode. In gas-
enees in body weight. However, there is tropods, however, this process could
a clear difference in the way these have happened more easily since
resources are used. Doriopsilla areolata lecitotrophic larvae often retain struc-
expends most resources producing tures used in the process of feeding
spawns with a high number of small (Strathmann, 1978).
eggs, and a very scarce gel matrix. Since planktotrophy is clearly the
Larvae hatch just a few days after egg most frequently observed deveiopment
mass deposition, as is typical for obliga- mode, Hadeield and Miller (1987)
tory planktotrophs, and thus not many assume that this is also the most primi¬
nutritivo reserves are needed. In opposi- tivo developmental strategy amongst
tion, D. pelseneeri produces a small opisthobranchs. They argüe that the
number of large, yolky eggs and a dense evolutionary direction will be towards
gel matrix in which they are embedded. lecithotrophic-planktonic deveiopment
The matrix is used for mechanical and, and from there to direct deveiopment, in
most certainly, for Chemical protection which the opisthobranchs with ameta-
of the embryos developing inside the morphic deveiopment are the most
egg-capsule. Since we did not have evolved forms. According to Todd
access to the complete reproductivo (2001), a larger egg should not be the
period, we were unable to calcúlate the trigger for this chango and for Hadfield
total reproductivo effort for these two AND Miller (1987) it is not clear if the
species and therefore to compare it with selectivo pressures responsible for this
others (e.g. Todd, 1979; DeFreese and have been the same in all opisthobranch
Clark, 1983; Gibson and Chía, 1991). species. Intense predation on early juve¬
Another conclusión arises from our niles could have selected for increased
results, larger adult specimens produce size, leading to a direct deveiopment
higher numbers of eggs per egg mass. mode, but in another situation the opis¬
This has been observed for both species thobranch can be the predator and may
studied herein. Allen, Krug and Mar- adapt its own life cycle to grow and
SHALL (2009) report for the sacoglossan reproduce before a short-living prey is
Elysia stylifera that larval size is deter- exhausted (Todd and Doyle, 1981). The
mined by the extra-capsular yolk, but not costs for this adaptation will be, in part,
by egg size. Todd, Lambert and Davies a reduction in opisthobranch size and
(2001), based on previous studies with fecundity, and production of larger,
Adalaria próxima (Alder and Hancock, lecithotrophic eggs or directly develo-
1854) (Lambert, Todd and Thorpe, ped offspring (pelagic larva could be
2000) generalise that between-population dispensable if prey is not too patchy)
variation in egg size is genetically deter- will be favoured (Hadfield and
mined. Such a pattern was not observed Miller, 1987). According to Todd (1991)
herein. Egg size appears to be species a consensus is lacking and probably
108
Calado ETal.: Reproduction in two sympatric Iberian nudibranch species
there are special cases for particular which produces the larger offspring sur-
species. vivorship even if it is energetically inef-
Planktotrophic species have a high ficient. However, as seen above, other
fecundity and great dispersal potential, authors claim that energetic factors
whereas species with direct develop- seems to be a lesser deterministic factor
ment have a reduced fecundity with a for the selection of developmental
higher larval stage protection and pattern.
usually hatch and settle in the same As Hadfield and Miller (1987)
places where their progenitors live already pointed out, there is "no valid
(ScHELTEMA, 1986). The data available reason to assume that species currently
on the two species herein studied found together evolved in sympatry or
support this idea. Doriopsilla areolata, under the conditions in which they are
with planktotrophic development, has a now found". Furthermore, it is not
wide geographic range whereas D. pelse- certain that planktotrophy and lecitho-
neeri, with direct development, has a trophy are different processes aiming at
much more restricted distribution, the same final results (Todd, 1991). We
mostly limited to the Iberian Peninsula are convinced that further phylogeo-
(see also Valdés and Ortea, 1997). graphic studies on the populations of
Potential dispersión capability of a Doriopsilla areolata and Doriopsilla pelse-
species is dependen! on many physical neeri will help to elucidate the origins of
and biological habitat conditions the speciation process and therefore the
(ScHELTEMA, 1986), however, and since evolutionary relationships between
both species feed on a variety of these two species.
sponges widespread in the Lusitanian
province (GC, personal observations),
no host constraint should be involved in ACKNOWLEDGMENTS
their actual distribution.
Studying two sympatric dorid nudi- We would like to thank Dr. Henrique
branchs with different larval strategies, Cabral for his help on statistical analy-
Todd (1979) claimed that planktotrophic sis. Fátima Martins and Peter Wirtz
species were 'Torced" into that develop- kindly provided the photos of the
mental mode since an insufficient spawn masses of D. areolata and D. pelse-
number of lecithotrophic eggs would be neeri that illustrate Figure 3A. The
produced to maintain its population sta- second author holds a grant from the
bility. This author also suggested that Fundaíjáo para a Ciencia e Tecnologia,
selection always favours the strategy Portugal (BD/82339/2011).
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