265
planktotrophic larvae, including selection for increased postmetamorphic survivorship (by producing large juveniles)
and selection for reduced larval mortality caused by predation and seasonal food fl uctuations (by shortening the freeswimming period) (see also Jablonski and Lutz 1983 ;
Nielsen 1995 , 1998 ; Clarke 1992 ; Jeffery 1997 ).
From this perspective, non-feeding larvae are more expedient if planktonic food availability is low and non-stable,
and vice versa. For instance, species of congeneric sea
urchins inhabiting opposite coasts of the Isthmus of Panama
have different egg sizes and larval types, refl ecting differences in productivity in the Pacifi c and Atlantic coasts of the
isthmus – planktotrophic larvae are found in the highly productive Pacifi c waters while lecithotrophic ones are characteristic of the Atlantic with a relative paucity of planktonic
food (Lessios 1990 ; Jaeckle 1995 ). Lessios ( 1990 ) suggested
that these differences in egg size are not a result of differences in the environment of the adults, but an adaptive
response to the primary productivity of the oceans in which
larval development occurs. At the same time, planktotrophy
can be retained if species switch to seasonal reproduction,
with periodic decreases in the amount of available food compensated for by correspondingly timed breaks in reproduction (see Todd and Doyle 1981 ).
With reference to Thorson’s rule, Jeffery ( 1997 ) suggested that multiple independent origins of lecithotrophy and
brooding in sea urchins in the Late Campanian–Maastrichtian
were associated with the gradual cooling of the ocean and
abrupt fl uctuations in phytoplankton abundance. These conditions, according to Jeffery, promoted the loss of planktotrophic larvae in at least nine sea urchin clades. Temperature
fl uctuations in the ocean in the very end of the Cretaceous
have been effectively proven (Barrera and Savin 1999 ), supporting Jeffery’s hypothesis. According to Emlet ( 1990 ),
echinoids lost planktotrophic larvae at least 14 times. To
note, brooders among living sea urchins are confi ned to the
cold, seasonal waters of the Antarctic and Subantarctic
(Emlet et al. 1987 ; Emlet 1990 ; McNamara 1994 ), with
brooding having originated independently in the Echinoidea
in these regions at least three times (Poulin and Féral 1996 ).
As for marine bryozoans, they may “reduce” planktotrophy in the process of colonizing non-stable estuarine habitats
(Dudley 1973 ). This hypothesis was based on a comparison
of the sizes and life spans of cyphonautes larvae in different
broadcasting cheilostomes (malacostegans) and on observations of their colonial development. So, based on Dudley’s
information about the whole life cycle of these epibionts, it
is reasonable to suggest that the transition from a long to a
short free-swimming larval period could be explained by the
shift to an “opportunistic” life strategy in unstable habitat
that involves a “shortening/accelerating” of both larval and
colonial development.
An opposing point of view concerning developmental
evolution would be that it is not larvae, but adults that are
“responsible” for the origin of a non-feeding mode. Chia’s
( 1974 ) hypothesis suggests that a transition to lecithotrophy
may be triggered by an acute shortage of resources. If less
food is available to adults, it is expedient to have fewer larvae/juveniles that are larger and develop faster. In other
words, if resources are scarce, populations decrease in number but this decrease is offset by a higher survival rate of
larvae/juveniles. Valentine (cited by Strathmann 1986 ) similarly suggested that the energy available to adults infl uences
the evolution of larval development (see also Clark and
Goetzfried 1978 ). Availability of food to parents during the
reproductive period was also considered in Todd and Doyle’s
( 1981 ) model.
Food is generally accepted to be the most important environmental factor infl uencing reproduction (see Strathmann
1986 ; Kasyanov 1989 ; Eckelbarger 1994 ). In many marine
invertebrates the quality of maternal nutrition is refl ected in
oocyte parameters such as size and content (see reviews by
Jaeckle 1995 ; Havenhand 1995 ). In particular, observations
and experiments on echinoids show that there is a correlation
between adult feeding and egg quality. In Strongylocentrotus
droebachiensis , eggs produced by individuals having plentiful or scanty food contained different amount of lipids
(Thompson 1983 ). Sea urchins Arbacia lixula taken from
habitats with different levels of food produced eggs of different size with different amounts of proteins and lipids; if there
was more food, the eggs were larger and contained more
yolk (George 1990 ; George et al. 1990 ; reviewed in Jaeckle
1995 ). Dependence on exogenous factors be seen in the data
of Krug ( 2007 ), who has shown that in winter and spring up
to half the individuals in the populations of the poecilogonic
snail Alderia willowi lay numerous small eggs from which
long-lived planktotrophic larvae develop, whereas in summer most snails lay a few large eggs from which lecithotrophic larvae develop. An increase in the number of snails
laying small eggs generally correlates with the cooling and
freshening of water. Thus, it seems that in summer abundant
food for adults facilitates production of large eggs and nonfeeding larvae with rapid development irrespective of the
abundance of plankton, whereas winter food depletion stimulates production of numerous eggs and planktotrophic larvae that will develop to juveniles and settle temporally nearer
to a summer period. A similar observation concerning the
correlation between food stability for adults and larval type
was made by Clark and Goetzfreid ( 1978 ).
Large-scale environmental changes are among the crucial factors that might induce changes in developmental
modes (Matsuda 1987 ; Levin and Bridges 1995 ; Jablonski
2005 ). Taking the Albian (that is, the beginning of the Late
Cretaceous diversifi cation of Cheilostomata) as the starting
point, we are faced with the onset of global biosphere
3.4 Causes, Stages and Consequences of Transition to Endotrophy in Cheilostomata and Ctenostomata
planktotrophic larvae, including selection for increased postmetamorphic survivorship (by producing large juveniles)
and selection for reduced larval mortality caused by predation and seasonal food fl uctuations (by shortening the freeswimming period) (see also Jablonski and Lutz 1983 ;
Nielsen 1995 , 1998 ; Clarke 1992 ; Jeffery 1997 ).
From this perspective, non-feeding larvae are more expedient if planktonic food availability is low and non-stable,
and vice versa. For instance, species of congeneric sea
urchins inhabiting opposite coasts of the Isthmus of Panama
have different egg sizes and larval types, refl ecting differences in productivity in the Pacifi c and Atlantic coasts of the
isthmus – planktotrophic larvae are found in the highly productive Pacifi c waters while lecithotrophic ones are characteristic of the Atlantic with a relative paucity of planktonic
food (Lessios 1990 ; Jaeckle 1995 ). Lessios ( 1990 ) suggested
that these differences in egg size are not a result of differences in the environment of the adults, but an adaptive
response to the primary productivity of the oceans in which
larval development occurs. At the same time, planktotrophy
can be retained if species switch to seasonal reproduction,
with periodic decreases in the amount of available food compensated for by correspondingly timed breaks in reproduction (see Todd and Doyle 1981 ).
With reference to Thorson’s rule, Jeffery ( 1997 ) suggested that multiple independent origins of lecithotrophy and
brooding in sea urchins in the Late Campanian–Maastrichtian
were associated with the gradual cooling of the ocean and
abrupt fl uctuations in phytoplankton abundance. These conditions, according to Jeffery, promoted the loss of planktotrophic larvae in at least nine sea urchin clades. Temperature
fl uctuations in the ocean in the very end of the Cretaceous
have been effectively proven (Barrera and Savin 1999 ), supporting Jeffery’s hypothesis. According to Emlet ( 1990 ),
echinoids lost planktotrophic larvae at least 14 times. To
note, brooders among living sea urchins are confi ned to the
cold, seasonal waters of the Antarctic and Subantarctic
(Emlet et al. 1987 ; Emlet 1990 ; McNamara 1994 ), with
brooding having originated independently in the Echinoidea
in these regions at least three times (Poulin and Féral 1996 ).
As for marine bryozoans, they may “reduce” planktotrophy in the process of colonizing non-stable estuarine habitats
(Dudley 1973 ). This hypothesis was based on a comparison
of the sizes and life spans of cyphonautes larvae in different
broadcasting cheilostomes (malacostegans) and on observations of their colonial development. So, based on Dudley’s
information about the whole life cycle of these epibionts, it
is reasonable to suggest that the transition from a long to a
short free-swimming larval period could be explained by the
shift to an “opportunistic” life strategy in unstable habitat
that involves a “shortening/accelerating” of both larval and
colonial development.
An opposing point of view concerning developmental
evolution would be that it is not larvae, but adults that are
“responsible” for the origin of a non-feeding mode. Chia’s
( 1974 ) hypothesis suggests that a transition to lecithotrophy
may be triggered by an acute shortage of resources. If less
food is available to adults, it is expedient to have fewer larvae/juveniles that are larger and develop faster. In other
words, if resources are scarce, populations decrease in number but this decrease is offset by a higher survival rate of
larvae/juveniles. Valentine (cited by Strathmann 1986 ) similarly suggested that the energy available to adults infl uences
the evolution of larval development (see also Clark and
Goetzfried 1978 ). Availability of food to parents during the
reproductive period was also considered in Todd and Doyle’s
( 1981 ) model.
Food is generally accepted to be the most important environmental factor infl uencing reproduction (see Strathmann
1986 ; Kasyanov 1989 ; Eckelbarger 1994 ). In many marine
invertebrates the quality of maternal nutrition is refl ected in
oocyte parameters such as size and content (see reviews by
Jaeckle 1995 ; Havenhand 1995 ). In particular, observations
and experiments on echinoids show that there is a correlation
between adult feeding and egg quality. In Strongylocentrotus
droebachiensis , eggs produced by individuals having plentiful or scanty food contained different amount of lipids
(Thompson 1983 ). Sea urchins Arbacia lixula taken from
habitats with different levels of food produced eggs of different size with different amounts of proteins and lipids; if there
was more food, the eggs were larger and contained more
yolk (George 1990 ; George et al. 1990 ; reviewed in Jaeckle
1995 ). Dependence on exogenous factors be seen in the data
of Krug ( 2007 ), who has shown that in winter and spring up
to half the individuals in the populations of the poecilogonic
snail Alderia willowi lay numerous small eggs from which
long-lived planktotrophic larvae develop, whereas in summer most snails lay a few large eggs from which lecithotrophic larvae develop. An increase in the number of snails
laying small eggs generally correlates with the cooling and
freshening of water. Thus, it seems that in summer abundant
food for adults facilitates production of large eggs and nonfeeding larvae with rapid development irrespective of the
abundance of plankton, whereas winter food depletion stimulates production of numerous eggs and planktotrophic larvae that will develop to juveniles and settle temporally nearer
to a summer period. A similar observation concerning the
correlation between food stability for adults and larval type
was made by Clark and Goetzfreid ( 1978 ).
Large-scale environmental changes are among the crucial factors that might induce changes in developmental
modes (Matsuda 1987 ; Levin and Bridges 1995 ; Jablonski
2005 ). Taking the Albian (that is, the beginning of the Late
Cretaceous diversifi cation of Cheilostomata) as the starting
point, we are faced with the onset of global biosphere
3.4 Causes, Stages and Consequences of Transition to Endotrophy in Cheilostomata and Ctenostomata