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ISSN 0018-8158, Volume 653, Number 1

SANTA ROSALIA 50 YEARS ON Review Paper

Winning the biodiversity arms race among freshwatergastropods: competition and coexistence through shellvariability and predator avoidance

Alan P. Covich

Published online: 15 July 2010

� Springer Science+Business Media B.V. 2010

Abstract Explanations for the coexistence of many

closely related species in inland waters continue to be

generated more than 50 years after Hutchinson’s

question: why are there so many kinds of animals?

This review focuses on the hypothesis that high

species diversity of freshwater gastropods results, in

part, from predators maintaining biodiversity across a

range of deep- and shallow-water habitats. Inverte-

brate predators, such as aquatic insects, and leeches

consume soft tissue of pulmonate snails by penetrat-

ing shells of various shapes and sizes. Crayfish and

large prawns chip around the shell aperture to enter

thick shells and crush small shells with their mandi-

bles. Crabs use their strong chelae to crush thin and

thick shells. Fishes with pharyngeal teeth are major

shell-breaking predators that combine with other

vertebrate predators such as turtles and wading birds

to increase the diversity of gastropod communities

by regulating the abundance of dominant species.

Although the generalized diets of most freshwater

predators preclude tight co-evolutionary patterns of

responses, there are combinations of predators that

modify gastropod behavior and shell morphology in

aquatic assemblages of different ages and depths. This

combination of invertebrate and vertebrate predatory

impacts led to competitive advantages among indi-

vidual gastropods with different adaptations: (1) less

vulnerable shell morphologies and sizes; (2) predator-

avoidance behaviors; or (3) rapid and widespread

dispersal with variable life histories. Some individuals

develop thicker and/or narrow-opening shells or shells

with spines and ridges. Other thin-shelled species

crawl out of the water or burrow to lower their risk to

shell-breaking or shell-entering predators. Some alter

their age at first reproduction and grow rapidly into a

size refuge. Fluctuations in water levels and intro-

ductions of non-native species can change competi-

tive dominance relationships among gastropods and

result in major losses of native species. Many different

gastropod predators control species that are human

disease vectors. Most snails and their predators

provide other ecosystem services such as nutrient

cycling and transfer of energy to higher trophic levels.

Their persistence and diversity of native species

require adaptive management and coordinated study.

Keywords Shell morphology � Aquatic insects �Leeches � Decapod crustaceans � Crabs �Crayfish � Fish � Omnivores � Invasive species �Disease ecology � Ancient lakes � Calcium �Water depth

Guest editors: L. Naselli-Flores & G. Rossetti / Fifty years after

the ‘‘Homage to Santa Rosalia’’: Old and new paradigms on

biodiversity in aquatic ecosystems

A. P. Covich (&)

Institute of Ecology, Odum School of Ecology,

University of Georgia, Athens, GA 30602-2202, USA

e-mail: alanc@uga.edu

123

Hydrobiologia (2010) 653:191–215

DOI 10.1007/s10750-010-0354-0

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Organisms interact with other organisms, both

conspecific and heterospecific, and their envi-

ronments; i.e., the evolutionary play takes place

within an ecological theater (G. E. Hutchinson,

1961).

Introduction

Although freshwaters comprise only 0.01% of the

Earth’s water and cover only 0.8% of the Earth’s

surface, these complex habitats contain about 6% of

all described species. Approximately 4,000 described

species of freshwater gastropods occupy many dif-

ferent continental and insular habitats around the

world (Covich, 2006; Strong et al., 2008). Compared

to the extent of marine and terrestrial habitats, this

disproportionately high species richness of gastro-

pods is also characteristic of many other freshwater

groups that stimulated G. E. Hutchinson’s numerous

contributions. As many of these organisms are

endemic species, they are highly vulnerable to global

extinctions in small, isolated springs and ponds as

well as in the larger lakes and rivers (Brown &

Johnson, 2004; Lydeard et al., 2004; Dudgeon et al.,

2006; Balian et al., 2008; Brown et al., 2008;

Crandall & Buhay, 2008; Brown & Lydeard, 2010).

Research on top-down controls on molluscan

species composition and dominance in a wide range

of communities demonstrates the importance of both

direct and indirect effects of predators. These studies

illustrate how a combination of invertebrate and

vertebrate predators can control different gastropod

assemblages. Most of the early studies of gastropod

predators focused on species in marine environments

where calcium is abundant, shells are often thick and

heavily structured (e.g., Palmer, 1979; Vermeij,

1987; Palmer, 1992; Cotton et al., 2004). Predator-

avoidance adaptations are also well documented in

these marine food webs (e.g., Rochette et al., 1998;

Cotton et al., 2004; Jacobsen & Stabell, 2004;

Bourdeau, 2009, 2010). In both marine and freshwa-

ters, many indirect, non-consumptive impacts as well

as direct consumption are known to alter how prey

populations respond to predators within the context of

complex food webs (Crowl & Covich, 1990; Bernot

& Turner, 2001; Rundle & Bronmark, 2001; Peckar-

sky et al., 2008). These species interactions are

important in sustaining ecosystems and their services

but generalizations are still lacking relative to most

benthic species regarding the value of sustaining

native species (Covich et al. 2004a, b; Giller et al.

2004).

A food-web perspective on biodiversity

As Hutchinson (1959, p. 147) noted ‘‘There is quite

obviously much more to living communities than the

raw dictum ‘eat or be eaten’ but to understand the

higher intricacies of any ecological system, it is most

easy to start form this crudely simple point of view.’’

Hutchinson’s focus on species richness and species

interactions in food webs continues to engage ecolo-

gists and evolutionary biologists because the sustain-

ability of freshwater biodiversity remains a challenge

as one of the most important questions in biology

(Dudgeon et al., 2006; Strayer, 2006; Cumberlidge

et al., 2009).

Early recognition that competitive exclusion could

reduce the number of coexisting species with highly

overlapping niches created a conundrum. Hutchinson

(1959, 1961) highlighted this recognition by question-

ing how it was possible that there are so many species

still competing in complex food webs when many

appeared to have highly similar fundamental niches.

This literature review focuses on identifying those

habitats, food webs, and conditions that are more

likely to support diverse species of gastropods than

others. The review examines the cumulative effects

of: (i) shell-crushing and shell-entering (penetrating)

predation by invertebrate and vertebrate predators;

(ii) environmental fluctuations on competition; and

(iii) prey avoidance behavior among thin-shelled

pulmonate species. Numerous experiments and long-

term observations demonstrate that the distribution of

gastropod species richness can be attributed to a

combination of biotic and abiotic features. Inter- and

intra-specific competitions can be influenced by

selective predation as well as by a lack of sufficient

concentrations of dissolved calcium or persistence of

well buffered, deep inland waters. These attributes

are widely documented geographically both in deep,

ancient lakes and in many other freshwater ecosys-

tems (e.g., Boss, 1978; Lodge et al., 1987; Økland,

1990; Hutchinson, 1993; Rundle et al., 2004; Turner

& Montgomery, 2009; Brown & Lydeard, 2010).

New information is integrated into these earlier

studies on how abiotic and physiological variables

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as well as introductions of non-native species can

alter the relative importance of adaptations to avoid

selective predation.

As discussed below, previous studies have dem-

onstrated that various top-down predatory influences

have a major effect on gastropod avoidance and

foraging behavior (Corr et al., 1984; Alexander &

Covich, 1991a, b; Dalesman et al., 2007, 2009a, b;

Wojdak, 2009), life history (Crowl, 1990; Crowl &

Covich, 1990; Crowl & Schnell, 1990), and shell

morphology (Vermeij & Covich, 1978; DeWitt,

1998, DeWitt et al., 1999, 2000, Krist, 2002, Johnson

et al., 2007). All these predator–prey interactions can

alter competitive outcomes among different gastro-

pod species. This review focuses first on several

widespread invertebrate (e.g., aquatic insects,

leeches, crayfishes, and crabs) and then on vertebrate

consumers (e.g., fishes and turtles) that are effective

shell-breaking or shell-entering predators on fresh-

water gastropods.

An ecosystem perspective on freshwater

gastropod biodiversity

Hutchinson (1993) noted the unique roles that lake

size (surface area, maximum depth), shape, history

and biogeography play in the distribution of many

highly diverse gastropod assemblages. He concluded

that ‘‘The prosobranch fauna of Tanganyika clearly

shows the greatest adaptive radiation found in the

gastropod fauna of any lake.’’ In this final publica-

tion, Hutchinson compared gastropod assemblages

among other deep, ancient and modern lakes to

explore which explanations might account the

remarkable variability in diversity and shell mor-

phology. It remains interesting but still unclear how

the most diverse assemblage of caenogastropod

(prosobranch) shell morphologies developed in Tang-

anyika, one of the oldest African Rift Valley lakes

(Cohen, 1994; Fryer, 2000; Wilson et al., 2004).

There is still no clear ecological explanation for

determining how the most seemingly ‘‘protected’’

species, Tiphobia horei, is well adapted to live in soft

sediments of this ancient lake with its large spines

and relatively thin shell (Fig. 1). Similarly, there is no

adequate ecological understanding of what might be

the adaptive nature of the cork-screw shaped shells

and opercula of the hydrobid gastropods of the

ancient Balkan Lake Ohrid (Albrecht & Wilke,

2008). Nor is it clear how the thick-shelled riverine

species Io fluvialis (Fig. 2), Tulotoma magnifera, and

Lithasia spp. in southeastern North America (Hersh-

ler et al., 1990; Ahlstedt, 1991; DeVries et al., 2003;

Minton & Lydeard, 2003; Minton et al., 2008)

evolved in response to isolation in drainage networks

and environmental variables.

Some well-studied examples of freshwater food

webs indicate that different predatory species seem to

play important roles in the predator–prey drama

taking place in Hutchinsonian evolutionary theaters

during a long series of ecological scenes and

intermissions. Each adaptive response to avoid active

predation during certain periods has tradeoffs and

variable costs and benefits that are context dependent

(e.g., Crowl & Covich, 1990, Alexander & Covich,

1991a, b; DeWitt, 1998; Hoverman & Relyea, 2007,

2009).

Several studies of gastropod shell variability

provide some clues as to which groups are winning

the arms race among the coexisting types of gastro-

pods and different types of predators. Numerous field

Fig. 1 Tiphobia horei from Lake Tanganyika is one of many

endemic species that have evolved in this ancient lake. It is an

iconic freshwater gastropod that represents the view that long

spines are likely the long-term evolutionary development of

predator-avoidance adaptation. Studies of how this species fits

into a general food web today remains to be undetermined. It is

not clear which predators may have driven this evolutionary

response (from: Livingstone 2003)

Hydrobiologia (2010) 653:191–215 193

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studies on ponds and lakes as well as controlled

laboratory experiments demonstrate differences in

how invertebrate predators attack their gastropod

prey and when prey respond with avoidance behav-

iors (e.g., selected examples in Table 1). Ancient

tropical lakes such as Tanganyika (Cohen et al.,

1997; Fryer, 2000), Ohrid (Albrecht & Wilke, 2008),

Lake Poso, and the Malili lakes on Sulawesi Island in

Indonesia (von Rintelen et al., 2004; Glaubrecht &

von Rintelen, 2008; Schubart & Ng, 2008; Schubart

et al., 2008) have unique assemblages of decapods

and fishes that consume gastropods.

Many invertebrate predators (aquatic insects,

leeches, crayfishes, and crabs) and vertebrate predators

(fishes, turtles) include gastropods in their diets. None

are completely specialized to feed exclusively on

gastropods. When their preferred molluscan prey is

unavailable, they switch to a wide range of other foods.

This foraging flexibility allows different potential

gastropod predators to remain in the food web and

often to subsist at relatively high levels of abundance.

In general, the selective forces on prey and

predators can be out of phase and asymmetrical. There

is often stronger pressure on the prey’s adaptation for

defense to avoid early mortality than for the predator

to switch prey and to avoid hunger unless the predator

is highly specialized (Nuismer & Thompson, 2006).

Most predators of gastropods are not limited to

particular types of prey, although sciomyzid fly larvae

are especially well adapted to feed on snail tissue

(Manguin & Vala, 1989). When gastropods are scare,

they can be opportunistic omnivores (e.g., Covich,

1977). These density-responsive food-web dynamics

occur in a wide range of waters, some of which are

very old and appear to be chemically and hydrolog-

ically stable. Other gastropod-based food webs are

common in highly variable, shallow waters.

Effects of non-native species on biodiversity

Increasingly, the spread of invasive, non-native spe-

cies of gastropods (Lodge et al., 1998; Contreras-

Arquieta & Contreras-Balderas, 1999; Albrecht et al.,

2009; Olden et al., 2009) and their predators (Hofkin

et al., 1991; Hofkin & Hofiner, 1992; Fuselier, 2001;

Smart et al., 2002; Dobson, 2004; Correia et al., 2005;

Strecker, 2006a; Bortolini et al., 2007; Foster &

Harper, 2007; Hernandez et al., 2008; Phillips et al.,

2009) is coupled with many other types of distur-

bances (Alin et al., 1999; Donohue et al., 2003; Cohen

et al., 2005; McIntyre et al., 2005; Strayer, 2010). The

potential for gastropod species to expand their ranges

of distribution is clearly related to their life histories

and how widely people transport them. Live-bearing

species and those that reproduce through self-fertil-

ization can disperse widely and displace other species

(e.g., Pointier et al., 1988; Covich, 2006).

Invasive, non-native species and other disturbances

potentially can cause the loss of important ecosystem

services such as food production and biological controls

of species that are vectors of human and wildlife

diseases (Dobson, 2004). Intentionally introduced spe-

cies may increase aquaculture production or serve as

temporary controls on disease vectors. These complex

relationships often require more detailed ecological

studies within a food-web context to determine the

likely tradeoffs related to intentional introductions (e.g.,

Mkoji et al., 1999; Gashaw et al., 2008).

An example of the need for detailed studies relates

to some of the earliest research on gastropod predators

that focused on native species of predators and

Pomacea as prey (Snyder & Snyder, 1971). Addi-

tional recent studies provide important perspective on

Fig. 2 Io fluvialis is another ionic species that was widely

distributed in the southeastern United States, especially in the

large rivers of east Tennessee. The snail has diminished in

distribution apparently because of disruption of the river flows

by construction of multiple dams and reservoirs as well as

other disturbances. The current predators are likely adult turtles

and raccoons, but detailed studies of these food webs are

lacking (from Robert T. Dillon, 2000)

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how native predators respond to availability of non-

native, invasive gastropod species. Research on how

various sizes and shapes of Pomacea are consumed by

different invertebrate and vertebrate predators pro-

vides information on the potential for natural controls

on an invasive gastropod, especially as related to

insights on general attributes of shell shape and size as

refugia from predation. Many different types of

invertebrate predators can consume juvenile snails

(typically less than 4 mm shell length), but fewer can

feed on adults. Their behavioral responses such as

burrowing during periods of lower water levels are

also of general interest.

Several species of Pomacea are dioecious and

have internal fertilization and high fecundity. Their

egg masses are laid above the water level where they

are not exposed to aquatic egg predators. The many

species of Pomacea are well adapted for burrowing.

They have both lungs and a ctenidium (gill) for

respiration in air and water. They are often spread

through aquarium suppliers and aquacultural intro-

ductions (Aditya & Raul, 2005, Aizaki & Yusa,

2009). Pomacea canaliculata can consume native

snails and may have large impacts on biodiversity in

some habitats (Kwong et al., 2009). There are more

than 25 native invertebrate and vertebrate gastropod

Table 1 Examples of invertebrate predators and their gastropod prey

Crush Enter Gastropod prey Shell size

(mm)

Avoid Source

Insect predators

Anax junius ?? ?? Physa acuta 1.0–3.0 Turner & Chislock (2007)

Abedus herberti ?? Physa virgata 4.0–12.0 Velasco & Millan (1998)

Belostoma flumineum ?? Physa virgata 3.5–5.5 Crowl & Alexander (1989)

Belostoma flumineum ?? Physa vernalis 2.5–5.5 Kesler & Munns (1989)

Belostoma flumineum ?? Physa acuta 1.0–2.0 Turner & Chislock (2007)

Belostoma flumineum ?? Physa gyrina ?? Wojdak (2009)

Belastoma flumineum ?? Helisoma trivolvis 1.0–10.0 Chase (1999)

Belostoma flumineum ?? Helisoma trivolvis Hoverman & Relyea (2007)

Dytiscus alaskanus ? Physa sp. Cobbaert et al. (2010)

Sepedon fuscipennis ?? Lymnaea palustris 2.0–4.5 Eckblad (1976)

Leeches

Glossiphonia complanata ?? Lymnaea peregra 3.2–14.9 ?? Bronmark & Malmqvist (1987)

?? Planorbis plannorbis 2.6–14.8 ?

Physa fontinalis 9.7 ???

Glossiphonia complanata ?? Helisoma anceps 1.0–2.0 Bronmark (1992)

Lymnaea emarginata 1.0–2.0

Physa gyrina 1.0–2.0

Nephelopsis obscura ?? Physa gyrina 8.0–11.0 ?? Brown & Strouse (1988)

Helisoma anceps 7.0–8.0

Helisoma trivolvis 7.0–10.0

Lymnaea emarginata 8.0–10.0

Crayfish predators

Orconectes virilis ??? Physella (=Physa) virgata 4.0–14.0 Crowl & Covich (1990)

Procambarus simulans ??? Physella (=Physa) virgata ???? Alexander & Covich (1991a, b)

Procambarus simulans ?? Planorbella (=Helisoma) trivolvis 4.1–16.0 ???? Alexander & Covich (1991a, b)

Procambarus acutus ??? Physa virgata 2.0–13.0 ???? Covich et al. (1994)

Procambarus clarkii ??? Physella heterostropha pomila 6.0–8.0 ???? McCarthy & Fisher (2000)

Methods of predatory attack and the presence or absence of predator-avoidance behaviors among various sizes of pulmonate prey

species

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predators known to include this invasive species in

their diets (Carlsson et al., 2004; Yusa et al., 2006;

Yoshie & Yusa, 2008; Carlsson et al., 2009; Burlak-

ova et al., 2010). Only the vertebrate predators

(fishes, turtles, and birds) and crabs can crush the

larger shells (e.g., Yusa et al., 2006). Other large,

thick-shelled invasive snails include Bellamya chine-

sis that is dispersing in North America and is likely to

affect food webs (Solomon et al., 2010).

Another well-studied example is the New Zealand

mudsnail, Potamopyrgus antipodarum, that has

spread rapidly in many temperate-zone lakes and

rivers in Australia, Europe, and North America

(Zaranko et al., 1997; Kerans et al., 2005; Loo et al.,

2007; Riley et al., 2008). These snails reach remark-

able densities ([10,000 individuals per meter) and can

create ‘‘no-analog’’ ecosystems that are distinct from

any seen before (Strayer, 2010). They are dispersed by

a number of mechanisms, the most difficult to reverse

is that adults can be ingested by fishes and survive

after being distributed long distances (Kerans et al.,

2005; Bruce & Moffitt, 2010). It is not clear if crayfish

predation will emerge over time as a potential control

of invasive mudsnails in some locations.

Besides the importance of native crayfish as

predators on non-native gastropods, several species

of crayfish (e.g., Procambarus clarkii and Cherax

quadricarinatus) are widely distributed through

aquaculture programs and these are invasive species

in many parts of world (e.g., Smart et al., 2002;

Bortolini et al., 2007; Foster & Harper, 2007).

Increased frequencies of introductions are leading to

multiple invasive species that can complement each

other’s niches. They can dominate inland waters

because their impacts on native species can be

compounded. This type of ‘‘invasion meltdown’’

enhances the chances for serial invasions by non-

native species (Ricciardi, 2001; Johnson et al., 2009).

A paleo-ecological perspective on biodiversity

As discussed below, climatically driven water-level

declines may have enhanced effectiveness of shell-

based and behavioral adaptations. Species coexistence

in these ancient ([100,000 years old) as well as in

other more recent inland aquatic ecosystems

(\10,000 years old) indicates that these biotic inter-

actions were often diverse and long-lasting. For

example, recent studies demonstrate that Lake

Victoria dried during the late Pleistocene

(\15,000 years ago) and then refilled to become a

site for rapid evolution of numerous species, espe-

cially cichlid fishes (Fryer, 2001; Elmer et al., 2009).

The connections among habitats during wet periods in

the African Rift Valley also may have been important

in determining dispersal among meta-populations and

meta-communities. Isolation during dry periods likely

increased changes in shell morphologies (Jørgensen

et al., 2007; Sengupta et al., 2009).

Based on several studies of fossil shells, the

diversity of many freshwater gastropods and some of

their predators are documented in large, deep habitats

as well as in waters of intermediate but variable depths

(Cohen, 1995). The number and geographic distribu-

tion of these paleolimnological studies, however, are

quite limited. As Cohen (2003, p. 324) notes,

‘‘…freshwater mollusks have received less attention

by paleo-ecologists than other groups of freshwater

fossils.’’ Some gastropod groups (such as the small

hydrobids) are widespread, abundant in the fossil

record, and morphologically complex. Extending the

temporal perspective on paleo–predator–prey relation-

ships will be valuable in understanding and managing

the rapidly changing freshwater habitats in the future

that experience various degrees of climatic change.

Adaptive traits among gastropods in inland waters

The physiological status of the prey species such as

levels of hunger or parasite infection can alter their

risk sensitivity and vulnerability to predation or their

competitive abilities in optimizing grazing and

reproduction (e.g., Dybdahl & Lively, 1996; Bernot,

2003; Gerald & Spezzano, 2005; Wojdak, 2009). In

many calcium-poor waters, freshwater gastropods are

thin-shelled and their ecological adaptations rely on

well-defined escape and avoidance behaviors (Bro-

dersen & Madsen, 2003; Rundle et al., 2004). Active

predation can cause some individuals to delay

reproduction and grow rapidly into a size refuge

(e.g., Crowl & Covich, 1990; Chase, 1999). These

types of adaptive traits allow a few species (e.g.,

Physa acuta) to be widespread (Dillon, 2000). These

species can often coexist with more localized thick-

shelled and spinose species as well as those that have

adapted shapes less vulnerable to shell-breaking or

shell-entering predators (Albrecht et al., 2009).

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Morphological traits

The importance of shell thickness, shape, and size is

well documented in the freshwater ecological litera-

ture (e.g., Vermeij & Covich, 1978; West & Cohen,

1996; DeWitt, 1998; DeWitt et al., 2000; Brown &

Lydeard, 2010). Most morphological complexity

among gastropods in inland waters is found in

ancient lakes and rivers with warm, calcium-rich

water. The striking morphological variability among

freshwater gastropod assemblages has generated

numerous discussions regarding their potential adap-

tive advantages in reducing risks of predation (e.g.,

Brooks, 1950; Boss, 1978; Vermeij & Covich, 1978;

Hutchinson, 1993; Strong et al., 2008). However,

there remain many unanswered questions regarding

tradeoffs among alternatives and rates of these

changes in sizes, shapes, and shell thickness. Some

traits such as shell thickness seem clearly to be

adaptive in reducing vulnerability to shell-breaking

predators. Gastropods have developed predator-resis-

tant shell morphologies in the same locations where

molluscivores were adapted to be shell-breaking or

shell-entering and penetrating consumers (e.g., West

et al., 1991; Dejoux, 1992; Nishino & Watanabe,

2000; Marijnissen et al., 2008).

When snail predators are abundant, heavy-shelled

or spinose species at least temporarily may provide a

competitive advantage over smaller, faster-moving

but more vulnerable, thin-shelled species. The trade-

offs relative to production, maintenance, and trans-

portation of a heavily armored shell compared to a

spinose or ribbed shell or those with a narrow

aperture or globose in shape remain under active

study (e.g., Michel, 1994, 2000; DeWitt et al., 2000;

Krist, 2002; Michel et al., 2004; Lakowitz et al.,

2008). These morphological adaptations require some

species to increase energy expenditures for locomo-

tion to carry heavier, stronger shells along the surface

or to burrow into sediments. These costs are a

tradeoff to offset the benefits of their decreased risk

of predation (e.g., Brown & DeVries, 1985; Bron-

mark, 1988; DeWitt, 1998; Nystrom & Perez, 1998;

Lewis, 2001; Turner, 2008). The costs of moving

upstream in flowing waters are especially increased

among spinose and/or large, thick-shelled species

because of increased drag. However, besides gaining

some advantages from reduced vulnerability to

predators, these larger, thicker shelled species may

have the added advantage of reduced vulnerability to

turbulent, storm flows in streams or wave surges in

lake-shoreline habitats.

Depending on the context, the various shapes and

sizes of shells provide different adaptive modes that

will be effective in reducing vulnerability to some

predators but not others. For any given size, thick

shells require sufficient calcium and take longer to

construct than thin shells with a narrow aperture. Yet,

these narrow openings can lower the chances of shell-

entering predators such as some aquatic insects (e.g.,

Anax junius, see Table 1) in grasping the snail foot

and extracting the soft tissue. However, other insects

such as Abedus herberti, Belostoma flumineum, or

Dytiscus spp. can still penetrate even narrow open-

ings. Small crayfish often begin to chip the thin edge

of a snail’s body whorl and attempt to enter the shell

through the aperture (Alexander & Covich, 1991a, b;

DeWitt, 1998). Larger crayfish can crush small snails

with their mandibles and attack larger thin-shelled

species by removing the shell apex, so that narrow

apertures have limited effectiveness among an array

of different types and sizes of predators. Larger and

globose-shaped shells are typically more difficult and

time-consuming for many shell-crushing predators to

handle (DeWitt, 1998; DeWitt et al., 1999). Increased

handling time can reduce optimal foraging and often

results in invertebrate predators dropping prey that

are then able to escape. Many vertebrate predators

such as fishes (e.g., McKaye et al., 1986; Osenberg &

Mittelbach, 1989; McCollum et al., 1998; Makoni

et al., 2004; Haag & Warren, 2006) and turtles (e.g.,

Vogt & Guzman, 1988; Bulte et al., 2008; Yoshie &

Yusa, 2008; Burlakova et al., 2010) are collectively

very effective at consuming a wide range of shell

thicknesses and shapes. Spines that widen the shell

likely deter relatively small, gap-limited, shell-break-

ing or shell-engulfing predators.

As discussed below, spinose shell morphologies

and/or shell thicknesses are found in ancient fresh-

water ecosystems such as in Lake Tanganyika, East

Africa (e.g., Tiphobia horei and Paramelania spp.),

in Lake Poso and Malili lakes on Sulewesi island,

Indonesia (Tylomelania spp.), and in Balkan Lake

Ohrid (e.g., Macedopyrgula spp.). These detailed

studies provide numerous insights to the importance

of decapods and fish predators in these complex food

webs (e.g., West et al., 1991; von Rintelen et al.,

2004; Albrecht & Wilke, 2008). The well-preserved

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gastropod assemblages in the fossil record offer

unique historical perspectives on the ecological

dynamics of shell development in understanding

how species coexistence relates to food-web structure

and variable habitats over long time scales (e.g.,

Cohen et al., 2005; Felton et al., 2007; Genner et al.,

2007).

In relatively shallow aquatic ecosystems, there are

many additional examples where persistent assem-

blages of gastropods with different shell characteris-

tics are distributed across a wide range of temporal

and spatial scales that illustrate dispersal and pred-

ator–prey dynamics (Lassen, 1975; Bronmark, 1985;

Lodge et al., 1987; Økland, 1990; Carlsson, 2000;

Turner & Montgomery, 2003, 2009). In non-glaciated

rivers such as the Duck River (Minton et al., 2008),

the Coosa River (DeVries et al., 2003), and the

Holston River (Ahlstedt, 1991) in southeastern North

America, there are examples of distinct shell mor-

phologies among Io fluvialis (Fig. 2), Tulotoma

magnifera, and Lithasia spp. In the Neotropics, there

are polymorphic gastropods (e.g., Mexipyrgus chur-

inceaus) in springs in Cuarto Cienegas, Mexico

(Fig. 3), and others (e.g., Pyrgophorus coronatus)

in lakes such as Laguna Chichancanab, in Mexico,

and Lago de Peten in Guatemala (Covich, 1976)

where they and their predators (fishes and decapods)

shift abundances over ecological time scales.

Behavioral traits

Behavioral responses are often observed among thin-

shelled gastropods when predators are actively feed-

ing. Examples include burrowing into sediments,

Fig. 3 Hydrobiid snail,

Mexipyrgus churinceanus,

collected from nearby

populations in Cuarto

Cienegas, Mexico, to

illustrate small-scale

variation in size and shell

pigmentation (A–C).

Herichthys minckleyipapilliforms (rightD) exhibit gill arches

modified into more gracile

pharyngeal jaws with small

muscles and pointed teeth

that are ineffective at

crushing snails while H.minckleyi molariforms (leftD) have robust muscles and

enlarged crushing teeth on

their pharyngeal jaws that

seem clearly modified to

crush snails. E portrays

heterogeneity in habitats

with Nymphaea (top) and

without Nymphaea (bottom)

(from Johnson et al., 2007)

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shaking to escape from a predator’s grasp, movement

to close refugia (crevices, under rocks), as well as

crawling into deeper waters or passively dispersing to

other more distant habitats by floating (catastrophic

drift). Life-history traits such high dispersal, fecun-

dity, delayed age at first reproduction to increase

growth rates provide highly flexible responses that

can diminish the risk of predation (e.g., Crowl &

Covich, 1990; DeWitt, 1998; Chase, 1999; Lewis,

2001; Krist, 2002; Turner, 2008). Continual dispersal

as ‘‘fugitive species’’ is an alternative mode of life-

history adaptation among thin-shelled species (Ver-

meij & Covich, 1978; Covich, 2006). Some species

diapause or form resistant resting stages so that they

can wait out stressful hydrologic events or periods

with low food resources and high risk of predation.

An array of experimental studies has evaluated

behavioral adaptations among thin-shelled gastropods

that avoid shell-breaking and shell-entering preda-

tors. For example, through both direct and indirect

effects, the presence of actively feeding crayfish

cause many pulmonate snails to crawl out of the

water, hide under substrata or to change their growth

rates and age at first reproduction (e.g., Bronmark,

1989; Alexander & Covich, 1991a, b; Covich et al.,

1994; Brown, 1998; Turner et al., 1999, 2000; Bernot

& Turner, 2001; Lewis, 2001; Turner, 2008; Brown

& Lydeard, 2010). These thin-shelled gastropod

species respond to species-specific chemical signals

and rapidly float to the water’s surface or crawl out of

the water in response to active crayfish predation

(Alexander & Covich, 1991a, b; Covich et al., 1994).

Early studies demonstrated that chemical cues trig-

gered different types of responses depending on

which predator was present (e.g., Snyder, 1967;

Snyder & Snyder, 1971). For example, Physa fonti-

nalis rapidly and consistently reacted by shaking their

shells once in contact with several species of

predatory leeches but they also responded to some

but not all non-predatory leeches (Townsend &

McCarthy, 1980). Recent studies have focused on

several types of predator-avoidance behaviors and

life-history responses (e.g., Dalesman et al., 2007,

2009a, b; Dickey & McCarthy, 2007; Dalesman &

Rundle, 2010). Neurobiological studies of predator

recognition are identifying physiological mechanisms

with increased precision (e.g., Orr et al., 2007, 2009;

Lukowiak et al., 2008). Other studies are determining

the tradeoffs in risk and vulnerability for not

responding under different environmental conditions

typical of food webs when predators interact with

their various gastropod prey (e.g., Turner & Mont-

gomery, 2009; Wojdak & Trexler, 2010).

Environmental complexity and constraints

on population dynamics

During extreme fluctuations in water levels, many

gastropods are subject to major changes in habitat

structure and resource availability. Some are at poten-

tially high risks of mortality while others avoid being

washed away or minimize aerial exposure and desic-

cation. Floods can displace and injure individuals not

well adapted for drifting during high flows. Some

gastropods move into structurally complex river banks

and lake shorelines where wave action and washout are

minimized. These responses allow gastropods to

reduce vulnerability to both hydrologically induced

mortality and many types of predators. Adaptations to

avoid predators may also simultaneously reduce

threats from physical stresses so that the same traits

can be effective in very different contexts. For

example, traits such as increased shell thickness and

rapid burrowing provide a ‘‘double defense’’ by

minimizing mortality from both hydrologic extremes

and shell-breaking predators. Adaptations to reproduce

quickly and disperse, or to hide once a predator begins

to consume snail prey, are other effective behavioral

adaptations to avoid active predators.

The permanence of water bodies is clearly of great

significance in allowing for the continued develop-

ment of gastropod diversity (e.g., Genner et al., 2007;

Schultheiss et al., 2009). The longer an inland aquatic

habitat can persist, the greater the chances are for the

number of gastropod species to increase by coloni-

zation and, possibly by speciation. Changes in

adaptive values of different types of shells are

hypothesized to be associated with infrequent,

large-scale fluctuations in water levels. As discussed

below, these changes in lake level can create habitats

where impacts of different types of invertebrate and

vertebrate predators can alter which gastropods

dominate the assemblages. For example, changes in

several lake levels determined by isotopic analyses of18oxygen of shells and other stratigraphic data

document some long dry periods and major changes

in distributions of gastropods (e.g., Covich & Stuiver,

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1974; Covich, 1976; Hodell et al., 2001, 2005).

Drought conditions can sever connections among

river drainage networks and especially among tribu-

taries entering lakes, some of which could connect

chains of lake basins. As water levels alter spatial

refugia, individual gastropods can develop distinctive

shell morphologies to minimize risks of predation

from a wide range of consumers. These major

changes in water levels are viewed as significant in

contributing to the predator–prey dynamics in iso-

lated populations in shallow-water pools and deltaic

habitats. The shoreline habitats of several tropical and

sub-tropical rivers and lakes are known to have

shifted in location in response to extreme climatic

changes over millennia (e.g., Cohen et al., 1997,

2005; Curtis et al., 1998; Felton et al., 2007; Genner

et al., 2007; Schultheiss et al., 2009). For example, as

discussed below, the endemic thiarid gastropods in

Lake Tanganyika are an exceptional radiation of

species that could likely have resulted from interac-

tions with evolving cichlid and crab predators and

with changes in water levels. Several studies docu-

ment changes in gastropod assemblages that provide

insights to how water-level changes likely alter

predator–prey interactions and gastropod distribu-

tions (Michel, 2000; West & Michel, 2000; Van

Damme & Pickford, 2003; Marijnissen et al., 2009).

Most freshwater ecosystems are small and shallow

and have a relatively low diversity of gastropods,

especially if they dry out intermittently (Turner &

Montgomery, 2009). Small bodies of water depend

on snail dispersal for colonization and community

assembly. Their levels of biodiversity can be esti-

mated using sizes of habitats and distances from

sources as in studies of island biogeography (Lassen,

1975; Browne 1981; Økland, 1990; Dillon, 2000;

Covich, 2006). Changing surface areas and water

depths require inclusion of hydrologic variability in

analysis of gastropod distributions because of the

major differences in respiration between pulmonate

(lung-bearing) and caenogastropod (gill-bearing) spe-

cies. In addition, hydrologic variability also influ-

ences their general life histories and vulnerability to

predators (Brown & DeVries, 1985; Lodge et al.,

1987; Crowl & Covich, 1990; Johnson & Brown,

1997; Brown et al., 1998; Dillon, 2000; Turner &

Montgomery, 2009; Brown & Lydeard, 2010).

Large, deep lakes and some deep rivers with

relatively high calcium concentrations infrequently

lower water levels that isolate sub-populations. These

are highly suitable ecosystems for gastropod speci-

ation, especially among the caenogastropods which

are capable of living at considerable depths. Baikal,

the oldest and deepest lake in the world, meets only

some criteria for having a high diversity of endemic

gastropods. This lake is the most persistent freshwa-

ter ecosystem on earth but the exceptionally deep,

cold water has low concentrations of calcium.

Consequently, this ancient basin is generally species

rich but relatively less diverse in gastropod species

than other groups (Kozhova & Izmest’eva, 1998).

The gastropods that have evolved in Baikal generally

have thin shells (e.g., Benedictia fragilis). Baikal has

an endemic gastropod family, the Baicaliidae, which

contains at least 148 species with 78% endemic. How

many of these thin-shelled species have evolved

behavioral adaptations to avoid predators is not

known. The extremely long history ([60 million

years) of this deep basin ([1700 m maximum depth)

suggests gastropods have likely evolved under a

range of different environmental conditions (Kozhov,

1963; Hausdorf et al., 2003), but most gastropods still

lack heavy shells. This lack of thick-shelled species

results in few groups capable of occupying the wave-

swept littoral zone. Most gastropod species live at

depths from 10 to 50 m even though some dissolved

oxygen is available throughout the deeper waters

(Sitnikova, 1994, 2006).

In contrast to Baikal and its cold, low-calcium

waters, the warm, calcium-rich waters in tropical

ecosystems with long growing periods provide ideal

conditions for gastropod population growth. In those

ecosystems where the water chemistry is enriched in

calcium, especially during drier periods when evap-

oration is high, the diversities of gastropods are likely

to be high if they persist over millennia. Prolonged

dry periods in generally wet basins are known to have

occurred in ancient lakes such as Tanganyika (Cohen

et al., 1997), Lake Malawi (Genner et al., 2007;

Schultheiss et al., 2009), and the Malili lakes on

Sulawesi island (von Rintelen et al., 2004; Glaubrecht

& von Rintelen, 2008). These ancient tropical lakes

have some of the highest species richness of gastro-

pods. Warm productive tropical waters often have

dense littoral-zone vegetation where gastropod den-

sities are generally very high and persistent.

Increased leaf surfaces among floating and sub-

merged macrophytes allow grazing on periphyton

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while also creating protective cover from many kinds

of predators.

Laboratory and field studies demonstrate that shell-

breaking molluscivores prefer thinner-shell prey. As

discussed below, the lower costs in terms of energy and

time expended for crushing and digesting thin shells

make some prey species more vulnerable to mollusci-

vores (Hoogerhoud, 1987; Brodersen & Madsen,

2003). Experimental studies demonstrate that some

gastropod species increase their growth rates and build

heaver shells when exposed to chemical signals from

predator fishes, and these increased shell-growth

responses are limited by the availability of calcium

(Rundle et al., 2004). Greater crushing resistance in

thicker shells is an advantage to gastropods in calcium-

rich waters, especially if their grazing and egg-laying

occur among macrophytes that provide additional

protection (e.g., Johnson et al., 2007).

Some ecosystems have calcareous sedimentary

deposits that form stomatolitic concretions by accu-

mulating layers of algae and cyanobacteria (Winsbor-

ough & Golubic, 1987). These bioherms are complex

in that mixtures of dead and live materials (snail

shells, ostracod valves, and charophytes) are covered

and encased in calcium carbonate over several years.

As plants grow and deposit thin layers of calcium

carbonate, these reef-like structures can grow quite

large (e.g., Cohen, 1989; Cohen et al., 1997). The size

and types of bioherms vary from the large, complex

forms and depth distributions observed in the larger

and much deeper Lake Tanganyika to smaller forms in

other basins such Laguna Chichancanab and Cuarto

Cienegas in Mexico. The biologically built structures

that occur in isolated desert springs of Cuarto

Cienegas (Winsborough & Golubic, 1987; Dinger

et al., 2006) have similar high concentrations of

calcium sulfate to those observed in Chichancanab.

These reef-like formations can dry out during low lake

levels and then reform once the water levels rise;

wave action can move them during storms and

rounded forms sometimes form in shallow waters

(Covich, personal observations). Heterogeneous sub-

strata such as stomatolitic bioherms may be important

in creating structural complexity and providing a wide

array of microhabitats that provide food (diatoms) and

cover for different shell morphs from predators. In

Chichancanab, crayfish excavate and hollow out the

concretions and use them for refuge. Habitat structure

influences how different predatory species search for

food and defend feeding territories in the shallow

littoral zones of lakes (e.g., Stevenson, 1992; Dinger

et al., 2006; Horstkotte & Plath, 2008; Plath &

Strecker, 2008).

Dense mats of charophytes as well as submerged

and floating macrophytes provide additional types of

structural complexity (e.g., Bronmark, 1989; Johnson

et al., 2007). These different types of floating and

submerged plants are important refuge from snail

predators for both thin- and thick-shelled grazing snails

(Covich & Knezevic, 1978; Lodge et al., 1987, 1994;

Covich, unpublished data). Periphyton growing on

charophytes and other plants provide food for snails in

these dense aggregations where visual predators

(fishes, wading birds, and turtles) are less effective.

Invertebrate predators (crayfish, insects, and leeches)

can be effective in these vegetated shorelines. In

general, the patterns of snail prey–predator distribu-

tions are determined by an integrated combination of

all the physical and chemical parameters within the

context of a full range of morphological and behavioral

traits that reduce vulnerability of all ages and sizes prey

(Covich, 1981; Covich et al., 1994). Differences in how

refugia and risk reduction change over time and space

allow multiple species to coexist. Various diverse

assemblages can accumulate over time within the

limits of calcium and other limiting resources

(Brodersen & Madsen, 2003; Rundle et al., 2004).

Top-down control by shell-breaking predators

Freshwater crabs, crayfish, prawns, and fishes are

effective snail predators in many types of freshwater

habitats and can exert top-down control on highly

diverse gastropod assemblages (e.g., West & Cohen,

1994, 1996; von Rintelen et al., 2004; Schubart &

Ng, 2008; Marijnissen et al., 2009). Freshwater

decapod crustaceans in particular consume a wide

range of foods (Hanson et al., 1990; Nystrom et al.,

1996; Parkyn et al., 2001; Zimmerman & Covich,

2003) but many species are especially well adapted to

chip and crush gastropod shells (Gherardi et al., 1989;

Alexander & Covich, 1991a; Snyder & Evans, 2006;

Brown & Lydeard, 2010; Covich et al., 2010; Hobbs

& Lodge, 2010). Diversity of crabs, crayfish, and

other decapods is limited by fish predation, low

calcium concentrations, restricted access to food and

cover as well as dispersal.

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The number of locations where crayfish, crabs, and

prawns overlap in the tropics is in need of further

study to determine how their feeding behavior and

general niche requirements differ, especially in terms

of any size-limits of prey when several species

consume gastropods. In Puerto Rico, there are many

locations and habitats where prawns (e.g., Macrob-

rachium carcinus, M. faustinum, and M. crenulatum)

and crabs (Epilobocera sinuatifrons) overlap and

consume some of the same resources (Covich,

personal observations). Rodrıguez (1986) suggested

that crabs and crayfishes do not overlap although

others have observed them to co-occur in several

lakes and rivers in Mexico such as Lake Chapala in

Jalisco, Lake Catemaco in Veracruz, and Rio Sabinal

in Tuxtla Gutierrez, Chiapas (Fernando Alvarez,

personal communication).

Crabs as predators

Five families of crabs are primarily found in tropical

and sub-tropical regions with at least 1,280 species

recognized and many more are likely still to be

described (Cumberlidge et al., 2009). Crabs in the

complex of five lakes and nearby Lake Poso on the

Indonesian island of Sulawesi have evolved a high

degree of endemism (Schubart & Ng, 2008; Schubart

et al., 2008). These endemic gecarcinucid crabs

influenced the diversity of endemic hydrobioid gas-

tropods (Haase & Bouchet, 2006) and pachychilid

gastropods (von Rintelen et al., 2004; Glaubrecht &

von Rintelen, 2008) in these lakes and adjoining

rivers. Another well-studied example is the evolution

of 10 species of crabs such as Platythelphusa armata

in the Potamonautidae (West & Cohen, 1994; Van

Damme & Pickford, 2003; Marijnissen et al., 2009) in

Lake Tanganyika is well documented. This assem-

blage illustrates how species of crabs have evolved in

lakes and rivers where[90 species of gastropods have

also undergone extensive evolution. A lag in decapod

responses to gastropod evolution of shell morpholo-

gies may have resulted in periods of a ‘‘unilateral arms

race’’ when only the gastropods responded. This

general asymmetry in response is typical of the

stronger pressure on prey than on the predator that is

widely observed (Nuismer & Thompson, 2006). Over

time, the crab chelae developed teeth that increased

the effectiveness of the claw to crush thickened

gastropod shells (Van Damme & Pickford, 2003).

Most freshwater crabs use their powerful chelae to

consume a wide range of plant and animal foods

(Dudgeon & Cheung, 1990; Zimmerman & Covich,

2003). Crabs use their chelae to carry snails’ short

distances to protective cover under large rocks and

into burrows. Once under protective cover, they can

chip away at the opercular edges of shells with their

mandibles without being vulnerable to their own

predators. Among the decapod crustaceans, only

crabs are adapted to crush shells with their strong

chelae as well as to use their mandibles to break

shells. Crabs also are able to orient and manipulate

shells to take advantage of pressure points in crushing

shells.

Juvenile crabs are often found in shallow waters

where crevices, detritus, and leaf packs provide

protective cover from their predators. Omnivorous

adults can feed on all sizes of snails with varied shell

thicknesses. These omnivores can persist even if they

reduce the number of gastropod prey to low numbers

by switching to other food sources. Some species are

highly amphibious and can feed on terrestrial snails

and seeds. They reach high densities where they can

avoid their predators in complexly structured habi-

tats. As pools in rivers and lakes dry out, crabs are

able to feed on high densities of snails concentrated

in shallow waters. Burrowing crabs are well adapted

to variable river flows and low lake levels. In many

substrata, crabs can persist during dry periods by

digging into groundwater and seeps and lowering

their metabolism until water levels increase (Covich,

personal observations).

Apparently, some African river-dwelling crabs can

be outcompeted by invasive crayfish (Foster &

Harper, 2007). In locations where crab densities

decline, major changes in gastropod assemblages can

be expected with rapid increases in fast-growing,

thin-shelled snail species that can rapidly disperse

into highly variable habitats. These changes have

implications for spread of human diseases such as

schistosomiasis and paragonimiasis that require snails

as intermediate hosts (Mkoji et al., 1999). Much of

what is known about the ecology of freshwater crabs

is based on studies associated with river blindness,

onchoceriasis, and the medical importance of their

roles as widespread predators in tropical waters and

their capacity to serve as sentinels for water quality.

Adult crabs can be subjected to intensive over-harvest

by humans although data on densities are scarce.

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Prawns as predators

There are more than 200 known species of the

freshwater shrimp Macrobrachium that are widely

distributed throughout the tropics and subtropics

(Bowles et al., 2000; Jayachandran, 2001; De

Grave et al., 2008). Most of these shrimp species

have amphidromous life cycles that require the

post-larvae to migrate upstream from estuaries to

grow and reproduce in rivers and lakes. Their

larvae drift downstream back to brackish waters

and molt into post-larvae to complete their com-

plex life cycle (Murphy & Austin, 2005; Kikkert

et al., 2009; Monti & Legendre, 2009). Some

larvae can drift in oceanic currents and thus many

of the species are widespread along coastal river

ecosystems. They can re-colonize rivers after

disturbances such as floods and droughts from

these coastal sources and are relatively resilient,

dominant consumers in many river food webs

(Covich et al., 2006, 2009). These omnivorous

decapods can grow quite large and live for more

than 8–10 years based on growth estimates (Cross

et al., 2008). Males of one of the largest species,

M. carcinus, can grow to 300 mm in length and

weigh up to kilogram.

Macrobrachium are effective predators on snails

and can create ‘‘shell middens’’ near the entrance

to their refugia; like crabs they hide during the day

under large rocks or in burrows and chip the edges

of larger shells that cannot be crushed immediately

with their mandiles (Covich, personal observations).

M. hainanense adult males consumed significant

amounts of the thiarid snail Brotia hainanensis in

their diet (Mantel & Dudgeon, 2004). Several other

studies (Barnish & Prentice, 1982; Lee et al., 1982;

Roberts & Kuris, 1990) have focused on predation

by Macrobrachium spp. on snails, primarily for

consideration of their use for biological control of

schistosome vectors. Macrobrachium and other

invertebrate predators are known to play combined

roles along with inter-specific competition among

non-native gastropods in controlling schistosome

vectors (Pointier et al., 1988). Covich (unpublished

data) observed Macrobrachium carcinus feeding on

planorbid snails (Biomphalaria glabrata) in labora-

tory studies and determined a size refuge existed in

a similar range ([4 mm shell length) as in previous

studies of crayfish.

Crayfish as predators

Globally, there are more than 640 crayfish species with

concentrations in North America and Australia. More

than 380 species occur in North America with species

richness concentrated in the southeastern North America

and in many different habitats (Crandall & Buhay,

2008; Hobbs & Lodge, 2010). As discussed above,

crayfish as gastropod predators are well documented

and are generally known to have omnivorous diets both

in their native and non-native ranges (Covich, 1977;

Lodge et al., 1994; Nystrom et al., 1996; Parkyn et al.,

2001; McCarthy et al., 2006; Johnson et al., 2009).

The roles that omnivorous crayfish play in exerting

top-down control on gastropod assemblages are well

documented (e.g., Lodge et al., 1994; Lewis &

Magnuson, 1999; Dickey & McCarthy, 2007). Cray-

fish overlap in their preferred habitats with many types

of gastropods. Crayfishes and prawns (such as Mac-

robrachium carcinus) chip and crush small snails but

are limited by the gape of their mandibles. Crayfish use

their well-developed chemoreception for two-dimen-

sional orientation to find food and mates as well as to

avoid predators (Covich et al., 1994).

More studies are needed on locations where crayf-

ishes overlap with freshwater crabs and shrimps to

determine how multiple species of decapod can affect

gastropod assemblages. These decapods appear to

compete with each other and may collectively have

significant impacts on gastropod prey. For example,

the native crayfish, Procambarus llamesii, in Laguna

Chichancanab are known to feed on small snails such

as Pyrgophrous coronatus and physids (Covich,

unpublished data), but field experiments are needed

to establish how their feeding compares with those of

the endemic pupfishes and other introduced fish

predators. As more non-native species are introduced

to this chain of lakes over time, a natural ‘‘laboratory’’

is available for comparative studies to evaluate these

impacts and suggest improved management of exotic

species.

Fish as specialized predators: studies

in neotropical waters

As discussed above, much of the literature on

molluscivores has focused on fishes in ancient lakes

in Africa (e.g., Fryer et al., 1985; McKaye et al.,

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1986; Fryer, 2000; Genner & Michel, 2003; Van

Damme & Pickford, 2003). The evolution of ciclids

in the African Rift Valley provide one of the best

studied radiations where some species of these fishes

developed specialized feeding behaviors and jaw

morphologies. These fishes are effective gastropod

consumers whenever gastropod prey are available,

but they can switch to other foods as do most all

freshwater predators. Other studies from North

America demonstrate the major role that gastropods

play in the diets of some fishes that are effective

shell-crushing predators (e.g., Osenberg & Mittel-

bach, 1989; McCollum et al., 1998; Mower & Turner,

2004). The relative importance of habitat structure as

spatial refugia for snails, especially the littoral-zone

macrophytes, is well established in these studies.

A few examples of fish predators from the

Neotropics are reviewed here to illustrate the similar

roles played by these fishes in relatively warm,

shallow-water ecosystems. Field experiments in Cu-

arto Cienegas, Mexico, demonstrate that hydrobid

snails (such as Mexipyrgus churinceaus) increase

threefold in density when predatory fishes (Herichthys

mincleyi and Cyprinodon bifaciatus) were excluded

(Dinger et al., 2006). In general, the evolution of

endemic hydrobid snails is often characterized by a

high degree of variability in shell thickness (Taylor,

1966; Hershler, 1984, 1985) that was associated with

the feeding by endemic molluscivorous fishes (Sage &

Selander, 1975; Trapani, 2003; Hulsey et al., 2006;

Johnson et al., 2007; Hulsey et al., 2008). Cichlasoma

minckleyi has highly variable pharyngeal jaw mor-

phologies that include some distinct morphs with

specialized broad, flat molariform teeth associated

with crushing snails (Fig. 3).

The cichlid evolution of pharyngeal adaptations for

crushing snails in northern Mexico at Cuarto Cienegas

is similar to some of the adaptations that have evolved

among several of the endemic pupfishes (Cyprinodon

spp.) in Laguna Chichancanab, in the Yucatan Pen-

insula of Mexico, that feed on Pyrgophorus coronatus

and other small mollusks (Humphries & Miller, 1981;

Stevenson, 1992; Strecker et al., 1996; Strecker

2006b). A fish-dominated food web (Fig. 4) illustrates

the generalized feeding of most of these endemic

fishes that consume a wide range of foods, especially

detritus. Whereas four of these seven species are well-

adapted to feed on snails, all of them are capable to

various degrees of sometimes feeding on these small

hydrobid snails. Only the largest species, C. maya,

feeds on smaller fish and on Physella cubensis

(U. Strecker, personal communication). Only C.

beltrani was observed to feed on charophytic algae.

Gambusia sexradiata also occurs in the lake and feeds

primarily on terrestrial insects that are carried into the

lake by wind and rain (Horstkotte & Strecker, 2005).

Similar snail species occur in Lago de Peten, farther

south in Guatemala, where salinity is lower and the

number of endemic fish species is not as high as in

Chichancanab; there are no known highly specialized

endemic molluscivores in Lago de Peten (Covich,

1976). As Chichancanab and other relatively young

karst lake basins such as Lago de Peten in Guatemala

(Covich, 1976; Curtis et al., 1998) often contain

similar but less specialized types of species interac-

tions, they provide insights to the rates of evolution and

the importance of multiple top-down controls over

gastropod assemblages that contrast to the well-

documented ancient lakes. Laguna Chichcankanab

(latitude: 19�53060�N, longitude: 88�4600�W) is

younger (most recently continuous for about 8,000

years) and smaller (20 km long and 600 m wide) than

other lakes (Covich & Stuiver, 1974; Hodell et al.,

2001, 2005) where flocks of endemic species of fishes

have evolved. Most endemic pupfishes occur in

isolated waters and not in multiple species or flocks

(Echelle et al., 2005).

In Chichancanab, fluctuations in lake levels during

just the last 8,000 years resulted in changes in water

chemistry and the evolution of seven endemic pupfish

species, with four species that have highly specialized

pharyngeal teeth and are adapted to feed on small

gastropods and bivalves (Humphries & Miller, 1981;

Stevenson, 1992; Strecker et al., 1996; Strecker,

2002; Horstkotte & Strecker, 2005; Strecker, 2005,

2006b). Unfortunately, the endemic species of pupf-

ishes in the Laguna Chichancanab are threatened by

the intentional introduction of tilapia and other non-

native species (Fuselier, 2001; Strecker, 2006a).

Laguna Chichancanab is dominated by highly

polymorphic gastropod species with variable shell

shapes and thicknesses (Pyrgophorus coronatus)

along with thin-shelled physid snails (Physella cub-

ensis). These snail prey are associated with both

predatory decapods (Procambarus llamesii) and sev-

eral endemic pupfish predators (Cyprinodon escond-

itus, C. maya, C. suaviun, and C. verecundus). The

shell variability among P. coronatus includes

204 Hydrobiologia (2010) 653:191–215

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different spinose morphs that increase the effective

size of these hydrobid prey relative to the gap width

of the predatory fishes and crayfish. These differences

in shell shape and spinosity influence how rapidly fish

and crayfish predators can consume small individuals

(\4 mm) and how many snails survive after handling

by the predator (Covich, personal observations).

Small thin-shelled physids are crushed immediately

while larger-shelled individuals are more slowly

chipped around the edge of the shell opening. Small-

and intermediate-sized hydrobid snails broken up and

the shell fragments not ingested. Some fish ingest the

entire snail and shell as readily observed by X-raying

the larger fishes (Covich, unpublished data).

During dry periods, this chain of lakes provides

periods of isolation that allow food-web dynamics to

continue with some different subsets of dominant

predators and prey as the water chemistry changes.

Samples of lake water taken intermittently since 1950

(Strecker, 2006a, b) indicated salinity changes in the

northern lake basin ranged from 3.5 to 5.6 PSU and

from to 1.2 to 2.9 PSU in the southern lake basin

(where groundwater apparently flows more fre-

quently into this sub-basin). The geomorphic features

of low relief and karst topography of the Yucatan

Peninsula result in complex, hydrologic connectivity

and variable lake levels. Rapid increases in ground-

water after tropical storms raise lake levels. Some of

C. beltrani

C. simus

C. esconditus

C. labiosus

C. maya

C. verecundus

C. suavium

DETRITUS

AQUATIC INSECTS

AMPHIPODS

OSTRACODS

GASTROPODS

BIVALVES

FISHES

Fig. 4 Food web based on

endemic Cyprinodon fishes

in Laguna Chichancanab

(modified from Horstkotte

& Strecker, 2005, p. 128)

Hydrobiologia (2010) 653:191–215 205

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these increases can follow rapidly after periods of

intense, hurricane-driven rainfall (Covich, personal

observations).

The high porosity, macro-pores, and complex flow

paths in this eroded limestone terrain also create

varied degrees of connectivity for periods of potential

colonization and dispersal. During wet periods when

the groundwater is relatively high, underground

streams can flow through caves and other connec-

tions, allowing subsurface movements of freshwater

organisms. Once these species occupy the intercon-

nected lakes and ponds, populations can become

isolated from other populations during dry periods or

if the connections are filled in with sediments.

Fluctuations between very wet, high lake levels to

prolonged dry periods with low lake levels resulted in

the lake shifting from a single continuous basin to a

chain of perhaps up to nine smaller, isolated lakes.

These fluctuations in habitat and isolation apparently

resulted in the evolution of seven endemic pupfishes

within this closed basin from a sister species,

Cyprinodon artifrons, a widespread coastal species

in Yucatan (Echelle et al., 2005).

Lake-level changes in Yucatan have been docu-

mented several times by use of stable isotopes 18O to16O (oxygen-18 and oxygen-16) from shell materials

extracted from cores of lake sediments (Covich &

Stuiver, 1974; Hodell et al., 2001). If temperature is

assumed to remain stable and the only inputs of water

are from precipitation and the outputs from evapo-

ration, then the ratio of 18O to 16O in lake water is

controlled mainly by the balance between evapora-

tion and precipitation in this closed lake. The 18O to16O ratio of lake water is at equilibrium with the same

ratios in the shells of live aquatic organisms when the

gastropods build shells of calcium carbonate

(CaCO3). Measuring the 18O to 16O ratio in gastropod

shells extracted from a series of sediment cores thus

provides a strong estimate of the changes in

evaporation/precipitation through time and is used

as a means to estimate lake level changes. Other

sources of information from lake sediments (e.g.,

changes in thickness of layers of organic and

inorganic materials) also document effects of pro-

longed dry and wet periods (including hurricanes) on

the biota of these inland karst ecosystems (Covich &

Stuiver, 1974; Curtis et al., 1998). This information

provides some baselines for studies of species

dispersal and evolutionary change since the last

major sea-level rise that resulted in raising the

groundwater and the lake levels.

Summary and future research

In order to explore how numerous freshwater gastro-

pod species continue to coexist over long periods, this

review focused on different types of predator–prey

interactions that can increase the diversity of gastro-

pod assemblages by reducing the dominance of any

one shell type or behavioral responses. These inter-

actions occur in many locations within a changing

context of highly variable water levels and climate.

Throughout the millennia, environmental conditions

in freshwater ecosystems altered water depths and

water chemistry. These changing conditions likely

influenced how different species adapted to changes in

the intensity and diversity of gastropod predators.

Long-term studies of large, deep ancient lake ecosys-

tems and smaller, younger ecosystems provide dem-

onstrate the importance of shell morphologies.

Simultaneously, there are effective behavioral adap-

tations, especially among some thick-shelled gastro-

pods, wherever their burrowing behavior lowers their

vulnerability to predators and to injury from storm

flows. If these gastropods feed on organic matter in

the sediments, then they can continue to grow but may

be somewhat limited in opportunities for mating when

population densities are low. Fugitive species have

adaptive life histories that include rapid dispersal and

high reproductive rates. Previous studies postulate

that extreme fluctuations in water levels in lakes and

rivers created periods of non-equilibrial environmen-

tal conditions. As in Hutchison’s ‘‘paradox of the

plankton,’’ these fluctuations in water levels likely

served as disturbances and changed benthic compet-

itive dominance relationships among gastropods.

Declines in water levels occasionally isolated popu-

lations, altered water chemistry, changed shoreline

habitats, and increased probabilities of encounters

with predators. Whenever gastropod prey were con-

centrated in shallow waters, increased opportunities

likely occurred for size-limited predation and benefits

for predator avoidance increased. The cumulative

effects of these shallow-water periods are hypothe-

sized to have influenced which diverse assemblages

persisted. Currently, the introduction of invasive

species and additional anthropogenic disturbances

206 Hydrobiologia (2010) 653:191–215

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are increasingly disrupting many diverse assemblages.

Some native predators consume non-native gastro-

pods but introduced predators create a potential threat

to native gastropods.

Although more paleoecological research on fossil

shell assemblages and hydrologic variability will

likely be highly insightful, more observations on

behavioral traits will also important to consider.

Predators that kill snails by penetrating the shell

opening, such as some leeches and aquatic insects,

leave no trace and their impact is difficult to determine

in remains of modern or fossil shells. Only controlled

experiments can evaluate their potential impacts. For

example, it remains to be determined if opercula

generally protect some species but not others from

shell-entering predators. Comparing the trade-offs

among various alternative ways that freshwater gas-

tropods have adapted to reduce risks of predation will

require an integrated approach and well-designed

comparative studies. Some greater degree of stan-

dardization of terminology and methodology will

enhance comparisons of experimental results.

Much uncertainty remains about how diverse

gastropod assemblages become parts of persistent

food webs. Top-down predator–prey interactions can

affect the potential for coexistence among gastropod

prey and predators, especially in ecosystems with

fluctuating water levels. As climatologists forecast

more extreme inter-annual variations in regional

patterns of precipitation, the consequences of floods

and droughts to these biotic interactions in rivers and

lakes will likely become increasingly complex. These

gastropod-based food webs provide important eco-

system services in recycling nutrients by grazing and

breaking down organic matter and in supplying food

to a diverse array of predators and to some people.

Gastropod predators are known to reduce snail vector

densities and play important roles in disease ecology.

They may also emerge as important predators in

minimizing the impacts of non-native gastropods and

other invasive species. Loss of these ecosystem

services and lower resiliency can result when well-

adapted native species are lost to localized extinction.

The ecological connectivity and coexistence of these

food webs will be complexly linked to how drainage

basins are managed in the future.

Acknowledgments I deeply appreciate Luigi Naselli-Flores’s

invitation to participate in this special issue. Professor G.E.

Hutchinson’s inspired and mentored many students and

ecologists. His remarkable intellectual contributions are to be

celebrated often! I also appreciate the help of many colleagues

who provided information about research on gastropod–

predator interactions. I especially thank J. E. Alexander,

K. M. Brown, T. A. Crowl, D. M. Lodge, and R. A. Stein and

G. J. Vereij for discussion of these ideas over the years.

F. Alvarez, J. Horstkotte, P. T. J. Johnson, M. Plath,

C. D. Schubart, and U. Strecker shared insights and ideas

from their recent studies. Two anonymous reviewers provided

helpful suggestions. Research support by the U.S. National

Science Foundation is greatly appreciated.

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Author Biography

Alan P. Covich (born 1942)

received his BS from

Washington University (St.

Louis) and MS and PhD

from Yale University in

ecology. He is a Professor

of Ecology and a former

director of the Institute of

Ecology at the University of

Georgia in Athens, Georgia,

USA. His research focuses

on effects of drought on

food-web dynamics in

insular and continental

streams. He currently serves

as president of the International Association for Ecology

(INTECOL) and is past president of the Ecological Society of

America, the American Institute of Biological Sciences, and

the North American Benthological Society. He is a North

American representative to the International Association of

Limnology. He co-edited three editions of the Ecology andClassification of North American Freshwater Invertebrates and

published reviews on freshwater ecosystems in Water in Crisis:A Guide to the World’s Freshwater Resources, the Encyclo-pedia of Biodiversity, the Encyclopedia of Inland Waters, and

the Encyclopedia of Hydrologic Processes.

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