Comparison of direct, indirect, and ecosystem engineering effects of an earthworm on the red-backed...

Ecology, 93(10), 2012, pp. 2198–2207� 2012 by the Ecological Society of America

Comparison of direct, indirect, and ecosystem engineeringeffects of an earthworm on the red-backed salamander

TAMI S. RANSOM1

Department of Biology, University of Virginia, Charlottesville, Virginia 22904-4328 USA

Abstract. In addition to creating or modifying habitat, ecosystem engineers interact withother species as predators, prey, or competitors. The earthworm, Lumbricus terrestris,interacts with the common woodland salamander, Plethodon cinereus, via: (1) ecosystemengineering, by providing burrows that are used as a refuge, (2) direct effects as a prey item,and (3) indirectly, by competing with microinvertebrates, another prey item for P. cinereus.Using enclosures in the forest, I examined the relative strengths of these component pathwaysbetween seasons and salamander age classes. I found that the relative strength (partial g2) ofthe positive direct (trophic) effect of L. terrestris on the change in mass of P. cineresus wasgreater than that of the negative indirect effect, but only in summer. Positive effects ofecosystem engineering were only evident over the winter as increased adult survival. Thisresearch has implications for how habitat provisioning complements more well-studied speciesinteractions, such as competition and predation, within communities.

Key words: competition; ecosystem engineer; effect size; habitat provisioning; indirect effects;interaction strength; Lumbricus terrestris; Plethodon cinereus; Mountain Lake Biological Station, Virginia,USA; predation; red-backed salamander; trophic effects.

INTRODUCTION

Although ecosystem engineers are typically studied

because they create or modify habitat (Jones et al. 1994,

Wright and Jones 2006), they may also interact with

other organisms as competitors, prey, or predators (e.g.,

Fukui 2001). For example, beavers alter the hydrology

of an area through the damming of streams (Rosell et al.

2005), but also change the composition of understory

plant communities through their browsing activities

(Parker et al. 2007). Understanding the relative impor-

tance of the different interactions between ecosystem

engineers and other organisms is an important step in

synthesizing knowledge about how habitat provisioning

complements more well-studied species interactions,

such as competition and predation, in shaping commu-

nities (Wright and Jones 2006).

The net effect of an ecosystem engineer on another

organism is also influenced by nonengineering pathways

(Wilby et al. 2001, Wilby 2002). For example, increasing

the complexity of understory vegetation provides

habitat for web-building spiders and indirectly decreases

abundances of aerial detritivores (Miyashita and Taka-

da 2007). In this case, the net effect of vegetation on

these insects was negative, even though there is no

discernable direct effect of vegetation complexity on

aerial detritivore abundance (Miyashita and Takada

2007). Determining the factors influencing the net effect

of an ecosystem engineer on organisms may be especially

helpful in cases where interactions occur via different

pathways (e.g., direct, indirect, or ecosystem engineer-

ing) and are of different signs. For instance, small carp

(Cyprinus carpio L.) increase phytoplankton and zoo-

plankton abundances through their bioturbation activ-

ities (Matsuzaki et al. 2007), and carp can also alter

zooplankton abundances directly through predation

(Parkos et al. 2003). Similarly, but at a community

level, crayfish (Paranephrops zealandicus) reduce densi-

ties of Tanypodinae by selectively preying on them while

Deleatidium mayflies are facilitated through the produc-

tion of fine particulate matter (Usio and Townsend

2004). Studies that consider the sign and strength of

both engineering and interspecific interactions when

evaluating net effects are only beginning to be per-

formed, but may clarify the roles of ecosystem engineers

in their communities (Wilby 2002).

In addition, the magnitude of trophic or ecosystem

engineering pathways can vary by season or the size

class of the ecosystem engineer. In the carp system

mentioned in the paragraph above, there are significant

differences in ecosystem engineering effects through

bioturbation based on carp size class (Driver et al.

2005). Likewise, the ecosystem engineering effects of

beavers could be expected to impact aquatic vegetation

throughout the year, while the negative effects of beaver

herbivory on flowering plants might be greater in the

spring or summer than in the winter (Rosell et al. 2005,

Parker et al. 2007).

Manuscript received 11 November 2011; revised 30 April2012; accepted 30 April 2012. Corresponding Editor: D. A.Wardle.

1 Present address: Department of Biology, Wabash Col-lege, 301 West Wabash Avenue, Crawfordsville, Indiana47933 USA. E-mail: [email protected]

2198

My general hypothesis is that, when two species

interact through both engineering and biotic pathways,

the relative strengths of these interactions will vary

temporally or among size classes (either of the engineer

or the ‘‘recipient’’ organism). Here I examined multiple

interaction pathways between the earthworm, Lumbricus

terrestris, and a common woodland salamander, Ple-

thodon cinereus. I chose to examine interactions between

these two species for several reasons. First, earthworms,

including the invasive L. terrestris, are well-known

ecosystem engineers that alter soil structure and

influence soil organic-matter content, nitrogen mineral-

ization, nutrient cycling, and other ecosystem processes

(Frelich et al. 2006). Second, salamanders are important

vertebrate predators in forest communities (Hairston

1987), with salamanders in the genus Plethodon often

identified as a dominant forest vertebrate (see review in

Davic and Welsh 2004). This species and other

salamanders in the genus Plethodon are often used as

bio-indicators of forest health (Petranka et al. 1993).

Third, L. terrestris and P. cinereus interact through both

ecosystem engineering and trophic pathways.

Lumbricus terrestris interacts with P. cinereus through

several pathways. Earthworms provide burrows that can

be used by P. cinereus as a refuge from predators or the

elements (Caceres-Charneco and Ransom 2010, Ransom

2011; see Plate 1). During the day, P. cinereus can be

found on the forest floor under rocks and logs, but it

spends much of its time underground (Bailey et al.

2004). Because individuals of P. cinereus are unable to

dig burrows (Heatwole 1960), they must rely on existing

retreats. Plethodon cinereus also consumes earthworms

(Maerz et al. 2005). Finally, L. terrestris may have

negative indirect effects on P. cinereus by reducing leaf

litter and competing with microinvertebrates, another

important prey item for P. cinereus (Maerz et al. 2009,

Eisenhauer 2010). The final net effect of earthworms on

P. cinereus likely depends on the relative strengths of

these positive (ecosystem engineering and direct trophic)

and negative (indirect competition) pathways. However,

salamander age class or season could alter strengths of

the three pathways. For example, juvenile P. cinereus

might not be able to consume any but the smallest L.

terrestris. However, ecosystem engineering effects could

be higher in the winter as P. cinereus is not freeze-

tolerant and earthworm burrows could provide an

important underground refuge (Storey and Storey 1992).

I used enclosures in a field setting to examine the

effect of L. terrestris on P. cinereus growth and survival;

through experimental manipulation I compared the

effects of L. terrestris as a habitat modifier, food source

for salamanders, and competitor. I predicted that the

relative strengths of these component pathways would

differ between seasons (summer vs. winter) and between

salamander age classes ( juvenile vs. adult). I predicted

that the underground habitat provided by earthworm

burrows would be more important over the winter than

the summer, and would affect adult and juvenile

salamanders similarly. I also predicted that, because

juvenile salamanders would not consume earthwormsreadily, the use of earthworms as prey would be more

important for adult than for juvenile salamanders.Finally, I predicted that consumption of leaf litter by

earthworms would lead to a reduction in microinverte-brate numbers, and that this indirect competition with

salamanders would be more important over the summerthan over the winter, but would affect adult and juvenilesalamanders similarly. The novelty of this project is that

it incorporates ecosystem engineering, direct (trophic),and indirect competitive effects within a single experi-

mental design so that the magnitude of the individualeffects can be compared. The exploration of the relative

strengths of interactions pathways is important forunderstanding how habitat provisioning complements

more well-studied species interactions, such as compe-tition and predation, in shaping communities.

METHODS

Experiments were conducted at Mountain Lake

Biological Station (MLBS), Giles County, Virginia,USA in the southern Appalachian Mountains at an

elevation of 1160 m. The forest is mixed deciduous, andthe forest floor leaf litter is dominated by northern redoak (Quercus rubra) and white oak (Q. alba). Salaman-

ders were kept in enclosures for 20 weeks over thesummer or over the winter, with new individuals

collected each season. The summer experiment ran from12 May–3 October 2009; the winter experiment ran from

7 November 2009–27 March 2010. The dates of theexperiments reflect typical seasonality at MLBS (e.g., the

last of the winter snow melted the week before 27March). On average, mean monthly temperatures peak

in July and August and are lowest from December–February; mean monthly precipitation generally is

highest in May and June and lowest in August andSeptember (Mountain Lake Biological Station Meteo-

rological Data; available online).2

I compared the following three effects of L. terrestris

on the growth and survival of P. cinereus over eachseason: (1) ecosystem engineering effects from burrow

creation, (2) direct effects as prey of P. cinereus, and (3)indirect effects through competition with microinverte-

brates. Adult L. terrestris build burrows that both adultand juvenile P. cinereus will use (Caceres-Charneco and

Ransom 2010, Ransom 2011), but are too large (100–1503 4 mm) to be consumed by P. cinereus. Thus, adult

earthworms exert ecosystem and indirect effects, but nodirect effects. Juvenile earthworms were expected to beeaten (i.e., a direct effect), but be too small to create

burrows that could be used by salamanders or toconsume large amounts of leaf litter and exert an

indirect effect.For each season, I examined the growth and survival

of P. cinereus in 108 small, deep enclosures consisting of

2 http://mlbs.org/metdata

October 2012 2199RELATIVE STRENGTHS OF INTERACTIONS

7.57-L (surface area¼ 0.05 m2) plastic buckets buried in

the ground. The soil in the forest surrounding MLBS is

very stony and comprised of sandy to very cobbly silt

loam, making it very difficult to bury even small

enclosures in the ground. Thus, the 7.57-L buckets were

the largest containers that could realistically be placed

deep enough into the ground with adequate replication.

Two adult L. terrestris were introduced into two-thirds

of the enclosures approximately two weeks before the

start of each experiment. Enclosures contained 45 cm of

soil, and, prior to earthworm introduction, soil was

homogenized and sifted through a 5-mm wire mesh to

remove any naturally occurring earthworms and co-

coons. The day before the start of the summer and

winter experiments, 20 mL of ‘‘hot mustard’’ solution

(20 g mustard powder mixed with 2 L water; adapted

from Hale et al. 2005) was applied to all enclosures and

all earthworms were removed. The next day, two adult

earthworms were reintroduced to one-third of the

enclosures; one-third of the enclosures then possessed

burrows for the duration of the experiment (i.e., an

ecosystem engineering effect), but no adult earthworms

(i.e., no indirect effects). Juvenile L. terrestris (2.5 g, or

;15 small juveniles) were added to half the enclosures

for a total of six treatments (Fig. 1). The amount of

juvenile earthworms (2.5 g/container ¼ 50 g/m2) was

chosen to reflect regional, published field data on

earthworm biomass (e.g., for the Piedmont region of

the southern Appalachian Mountains, Callaham and

Hendrix 1997; for Maryland, Szlavecz and Csuzdi 2007)

and local field observations for juvenile earthworm

densities in May. Because earthworm biomass fluctuates

with season, the 2.5 g of juvenile earthworms likely

underrepresented natural densities in summertime and

overrepresented natural densities over the winter.

After earthworms were introduced to the appropriate

treatments, 65 g of dry leaf litter and its associated

microinvertebrates, one ceramic tile as a cover object

(10.2 3 10.2 cm), and either an adult or juvenile

salamander (n¼ 9 for each age class for each treatment)

were added to each enclosure. This density of P. cinereus

in the buckets was about three times the average density

of salamanders reported in some years (6.55 salamander/

m2 in 2006; Buderman and Liebgold 2012). However, the

‘‘high’’ densities in the enclosures are closer to the actual

‘‘salamander to habitat ratio’’ because, unlike my

enclosures, these and other published density data include

unsuitable space and poor habitat (e.g., bare ground,

trees, and rocks that contain few prey items; Roberts and

Liebgold 2008). The leaf litter, primarily consisting of Q.

rubra and Q. alba, was collected from the forest floor,

homogenized, and air-dried one week before weighing.

The amount of leaf litter added to the enclosures (65 g)

was about three times the amount of average leaf litter

found in the forest (but containing a volume that

matched the highest levels found in the forest; T. S.

Ransom, unpublished data), corresponding to the amount

of leaf litter per salamander based on published

salamander densities (Buderman and Liebgold 2012).

The enclosures were then covered with mesh screening in

order that they would contain salamanders and earth-

worms, and exclude predators, but otherwise be exposed

to natural forest conditions. Finally, the enclosures were

sealed with all-weather silicone, and bamboo stakes were

arranged in a teepee around enclosures to deter deer.

Salamanders were collected from Jefferson National

Forest approximately one week prior to the start of an

experiment and stored in individual sealed plastic bags

with damp leaf litter. Leaf litter was removed from bags

and replaced with a moistened paper towel 48 h before

salamanders were to be placed in enclosures. Salaman-

ders were weighed ;24 h before being placed in

enclosures; snout–vent length (SVL) was measured three

times and the average calculated.

After 20 weeks, enclosures were dismantled. Remaining

leaf litter was placed in individual, lidded plastic tubs (30

3 15.5 3 8.5 cm) with a Sticky Trap (6 3 8 cm; Great

Lakes IPM, Vestaburg, Michigan, USA) overnight. After

24 h, the sticky traps were removed and stored until

microinvertebrates could be identified under a 1003

stereomicroscope; leaf litter was air dried for one week,

and then massed. Earthworms and salamanders were

removed from enclosures; salamanders were placed in

individual sealed plastic bags with a moistened paper

towel and massed the next day before being returned to

their original points of capture. If a salamander could not

be found after carefully sifting through an enclosure’s soil

and the enclosure was still completely sealed, the

salamander was recorded as dead (skeletal remains were

FIG. 1. Study design of the six treatments used to test howthe earthworm, Lumbricus terrestris, interacts with the commonwoodland red-backed salamander, Plethodon cinereus. Illustra-tions represent the earthworm treatment(s) (i.e., earthwormburrow, adult earthworms, or juvenile earthworms) for eachenclosure. The terms within each box indicate whetherecosystem engineering, indirect, or direct effects of earthwormson salamanders were present in each treatment. Note thatindirect effects could not be entirely separated from ecosystemengineering effects. Half of the enclosures (n ¼ 54) housed asingle adult salamander, and half housed a single juvenilesalamander.

TAMI S. RANSOM2200 Ecology, Vol. 93, No. 10

also sometimes found). If, however, an enclosure was not

completely sealed, data from that enclosure was not used

in analyses.

All data were analyzed using SAS/STAT Version 9.1

(SAS Institute 2004). General linear models (proc

GLM) analyzed the proportional change in mass of

juvenile or adult P. cinereus over the summer or winter

with ecosystem engineering (0 or 1), indirect (0 or 1), and

direct (0 or 1) effects as independent variables; block was

considered as a random effect. Two interactions were

also included in the model: an ecosystem engineering 3

direct effect interaction, and an indirect effect 3 direct

effect interaction. An ecosystem engineering 3 indirect

effect interaction could not be included because indirect

effects were tied to the presence of adult earthworms

that also exerted ecosystem engineering effects. (Note: to

assure that the incomplete design did not affect the

results, I ran the analyses again using only enclosures

within the direct and ecosystem engineering complete

block design. The results are not reported here, but were

nearly identical for those interactions as when indirect

effects were included in analyses). Interactions were

removed from the model for P . 0.25. Average initial

SVL (mm) of salamanders was included as a covariate.

Magnitudes of effect (partial g2) were calculated to

provide a measure of the percentage of variance in

proportional change in mass of salamanders that was

uniquely attributable to each independent variable.

Logistic regressions analyzed the survival (0 or 1) of

adult and juvenile salamanders over the winter; indepen-

dent variables, interactions, and the covariate were the

same as the GLM analyses in the paragraph above with

interactions removed if P . 0.25 (proc LOGISTIC).

Survival data for summer were not analyzed as survival

over the summer was near 100%. Separate analyses were

conducted for adult and juvenile salamanders for both

the summer and winter data in the following analyses.

The amount of leaf litter (g) remaining in enclosures and

the number of microinvertebrates found on sticky traps

were analyzed using GLMs with a gamma and negative

binomial distribution of errors, respectively (proc GLIM-

MIX). Independent variables and interactions were the

same as the previous analyses, although the SVL of

salamanders was not included as a covariate; interactions

were removed if P . 0.25. GLMs with a negative

binomial distribution of errors (proc GLIMMIX) were

used to compare the number of juvenile earthworms

recovered in treatments with earthworms.

RESULTS

During the summer experiment, 41 of 54 adult and 40

of 54 juvenile enclosures remained sealed over the 20

weeks. Failure of seals to remain intact often appeared

to result from deer damage. All adults survived in the 41

sealed enclosures; skeletal remains of four juvenile

salamanders were found in sealed enclosures. The

GLM for proportional change in mass for adult

salamanders explained 73% of the variation in the data

(R2 ¼ 0.73, F5,35 ¼ 19.32, P , 0.0001). Adult

salamanders gained more mass over the summer when

juvenile earthworms were present in enclosures (i.e.,

through a positive direct effect as food) than when

juvenile earthworms were not added to enclosures

(Table 1, Fig. 2a). Indirect effects negatively affected

TABLE 1. General linear model (GLM) results for proportional change in mass for adult and juvenile red-backed salamandersPlethodon cinereus, amount of leaf litter remaining in enclosures, and number of microinvertebrates in leaf litter over the summerand winter.

Summer Winter

Adult Juvenile Adult Juvenile

Parameter df F P df F P df F P df F P

Proportional change in mass

EE 1, 35 2.69 0.110 1, 31 0.11 0.747 1, 32 0.76 0.391 1, 25 1.06 0.314IE 1, 35 6.45 0.016 1, 31 1.20 0.281 1, 32 0.10 0.749 1, 25 3.21 0.085DE 1, 35 74.10 ,0.001 1, 31 4.99 0.033 1, 32 2.50 0.125 1, 25 2.59 0.120EE 3 DE 1, 35 � � � � � � 1, 31 � � � � � � 1, 32 � � � � � � 1, 25 3.63 0.068IE 3 DE 1, 35 1.93 0.174 1, 31 � � � � � � 1, 32 � � � � � � 1, 25 � � � � � �SVL 1, 35 1.80 0.189 1, 31 58.46 ,0.001 1, 32 0.12 0.738 1, 25 5.71 0.025

Leaf litter remaining

EE 1, 36 1.05 0.313 1, 34 2.08 0.159 1, 38 2.06 0.159 1, 35 0.06 0.811IE 1, 36 58.61 ,0.001 1, 34 67.83 ,0.001 1, 38 4.96 0.032 1, 35 0.76 0.390DE 1, 36 2.75 0.106 1, 34 32.14 ,0.001 1, 38 0.00 1.000 1, 35 0.15 0.703IE 3 DE 1, 36 5.04 0.031 1, 34 16.35 ,0.001 1, 38 1.87 0.180 1, 35 � � � � � �

Microinvertebrates

EE 1, 36 0.14 0.713 1, 31 0.00 0.976 1, 38 1.51 0.227 1, 34 1.05 0.313IE 1, 36 15.38 ,0.001 1, 31 6.27 0.018 1, 38 4.05 0.051 1, 34 0.11 0.745DE 1, 36 5.44 0.025 1, 31 6.57 0.015 1, 38 2.82 0.101 1, 34 0.04 0.836EE 3 DE 1, 36 2.10 0.156 1, 31 � � � � � � 1, 38 � � � � � � 1, 34 1.69 0.202

Notes: Abbreviations are: EE, ecosystem engineering effects; IE, indirect effects; DE, direct effects; and SVL, snout–vent length.Ellipses indicate that interactions were removed from models (because P . 0.25). Boldface values indicate significant effects (P ,0.05). See Fig. 1 for study design.


the change in mass of adult salamanders, with adults

losing ;2.5 times more mass when adult L. terrestris

were present in enclosures compared with controls or

enclosures with only burrows (i.e., through a negative,

indirect effect; Table 1, Fig. 2a). The GLM for

proportional change in mass for juvenile salamanders

explained 75% of the variation in the data (R2 ¼ 0.75,

F4,31¼ 19.41, P , 0.0001). Although indirect effects did

not affect juvenile growth, juvenile salamanders gained

twice as much mass over the summer when juvenile

earthworms were added to enclosures than when they

were not (Table 1, Fig. 2b). The initial size of juvenile

salamanders also influenced proportional change in

mass, with smaller salamanders growing more (Table

1). Partial g2 showed that the direct effects of juvenile

earthworms accounted for most of the variation in the

change in mass of adult salamanders, whereas initial size

(SVL) of juveniles accounted for the majority of

variation in the growth of juvenile salamanders during

the summer (Fig. 2e).

During the winter experiment, 43 of 54 adult and 38

of 54 juvenile enclosures remained sealed. The GLM for

proportional change in mass for adult salamanders was

not significant (R2 ¼ 0.13, F4,32 ¼ 1.04, P ¼ 0.405);

FIG. 2. (a–d) Proportional changes in mass (mean 6 SE) for adult salamanders over the (a) summer and (c) winter and forjuvenile salamanders over the (b) summer and (d) winter. Abbreviations are: EE, ecosystem engineering effects; and IE, indirecteffects. Solid symbols represent direct effects (i.e., juvenile earthworms) present; and open symbols represent no direct effects (i.e.,no juvenile earthworms) present. (e, f ) Magnitudes of effect (partial g2) over the (e) summer and (f ) winter showing the measure ofthe percentage of variance in proportional change in mass (g) of salamanders accounted for by ecosystem engineering effects (EE),indirect effects (IE), direct effects (DE), and initial size (snout–vent length, SVL). Bars with a bold outline and an asterisk (*) abovethem indicate factors that were significant (P , 0.05) in the general linear models (GLMs).


ecosystem engineering, indirect, and direct effects did

not affect proportional change in mass of adult

salamanders over the winter (Table 1, Fig. 2c). Similarly,

the GLM for proportional change in mass for juvenile

salamanders was not significant (R2¼ 0.29, F5, 25¼ 2.04,

P¼ 0.108). Although none of the main effects influenced

the proportional change in mass of juvenile salamanders

over the winter, the effect of initial SVL was significant

with smaller juveniles growing more (Table 1, Fig. 2d).

However, the partial g2 the initial size of juveniles

accounted for ,20% of the variation in the growth of

juvenile salamanders over the winter (Fig. 2f ).

Adults did not survive over the winter in 10 of 43

sealed enclosures and juveniles did not survive in 8 of 38

sealed enclosures. Adult salamanders were 14.36 times

(95% Wald confidence limits, 1.2–168.1) more likely to

survive the winter when earthworm burrows were

present, either with or without adult earthworms

compared to controls with or without juvenile earth-

worms (v2¼ 4.51, P¼ 0.034; Fig. 3a). The indirect effect

(v2 ¼ 0.14, P ¼ 0.712) and direct effect (v2 ¼ 0.40, P ¼0.528) did not influence survival over the winter (Fig.

3a), nor did initial SVL (v2 ¼ 1.73, P ¼ 0.189). Juvenile

survival over the winter was not affected by ecosystem

engineering (v2¼ 0.12, P¼ 0.729), indirect (v2¼ 0.69, P

¼0.407), or direct (v2¼0.42, P¼0.515) effects (Fig. 3b).

Initial SVL also did not influence juvenile survival (v2¼0.59, P ¼ 0.443).

To further examine the indirect interaction pathway, I

measured final leaf litter mass (g) remaining in

enclosures and the number of associated microinverte-

brates (Table 2). Over the summer, indirect effects and

the interaction between direct and indirect effects

influenced the amount of leaf litter remaining and

microinvertebrates present in enclosures with adult

salamanders, with less leaf litter remaining and fewer

microinvertebrates found in enclosures with adult

earthworms (Table 1, Fig. 4a). The amount of leaf litter

FIG. 3. Proportion (mean 6 SE) of (a) adult and (b) juvenile salamanders surviving over the winter. Abbreviations are: EE,ecosystem engineering effects; and IE, indirect effects. Solid symbols represent direct effects (i.e., juvenile earthworms) present, andopen symbols represent no direct effects (i.e., no juvenile earthworms) present.

TABLE 2. Number of microinvertebrates and amount of leaf litter (g) remaining in the enclosuresat the end of the experiment (mean 6 SE).

Number of microinvertebrates Leaf litter remaining (g)

Experimental treatment Direct effect No direct effect Direct effect No direct effect

Adult, summer

Control 5.4 6 3.0 17.3 6 5.2 21.3 6 9.3 41.9 6 7.5Ecosystem engineering 8.5 6 1.9 8.3 6 2.7 26.0 6 5.0 52.0 6 13.5EE þ IE 1.6 6 0.8 2.9 6 1.4 7.8 6 1.6 7.0 6 1.9

Juvenile, summer


Adult, winter


Juvenile, winter


Note: Abbreviations are: EE, ecosystem engineering effect; and IE, indirect effect.


that was consumed in enclosures with adult earthworms

over the summer was striking; however, salamanders

from all treatments had some prey in their stomachs at

the end of the experiment (stomach contents are visible

when salamanders are held up to a light to ‘‘candle’’

them). For enclosures with juvenile salamanders, direct

and indirect effects reduced the amount of leaf litter

remaining and the number of microinvertebrates pres-

ent, indicating that, over the summer, unconsumed

juvenile earthworms were depleting the leaf litter and

associated microinvertebrates (Table 1, Fig. 4b). In the

winter experiment, there was an indirect effect of

earthworms on the amount of leaf litter remaining in

enclosures with adult salamanders, although this did not

effect change in mass of adult salamanders (Table 1); no

other factors were significant in the adult or juvenile

models over the winter (Table 1).

At the end of the summer experiment, the age class of

the salamander significantly affected how many juvenile

earthworms were recovered from enclosures in with a

‘‘direct effect’’ treatment (F1,38¼8.02, P¼0.007). Nearly

twice as many juvenile earthworms were recovered from

enclosures with juvenile salamanders compared with

enclosures with adult salamanders (6.84 6 0.87 and 3.82

6 0.63 for juveniles and adults, respectively [mean 6

SE]). The same trend was not found in the winter

experiment (F1,37¼ 0.61, P¼ 0.441) with the number of

juvenile earthworms recovered similar across salaman-

der age classes (2.56 6 0.27 and 2.28 6 0.35 for juveniles

and adults, respectively).

DISCUSSION

Studies of ecosystem engineers have only rarely

integrated effects through biotic pathways, and many

studies examine only the net effects of engineering

organisms on other species (Wilby et al. 2001).

However, when the strength of interaction pathways

vary, whether seasonally, based on life stage, or other

abiotic or biotic conditions, this implies that the net

effect of one species on another may change in both

direction and magnitude in different circumstances.

Here I found that the net effect of the burrowing

earthworm, L. terrestris, on adult and juvenile P.

cinereus was positive. Overall, the presence of earth-

worms benefits salamanders and all the pathways I

examined (i.e., ecosystem engineering, direct, and

indirect) contributed to either salamander mass change

or survival. But, as expected, some effects were stronger

than others, and the relative strengths of these effects

varied depending on season and salamander age class.

Summer is an important time period for growth and

sequestering energy and fat stores for many animals,

including P. cinereus. Indirect effects of earthworms,

through the consumption of leaf litter, reduced the

microinvertebrate prey of salamanders and negatively

affected the proportional change in mass of adult

salamanders during the summer. This effect, however,

was small compared to the direct effect of juvenile

earthworms as prey, which accounted for three times the

variation in the change in mass of adult salamanders

over the summer compared with the indirect effect of

adult earthworms. And, while both adult and juvenile

salamanders benefited by having juvenile earthworms in

enclosures over the summer, the positive direct effect of

earthworms as prey was greater for adult compared with

juvenile salamanders; initial size (SVL) accounted for

most of the variation in growth for juvenile salaman-

ders. The benefits of earthworm ecosystem engineering

for salamanders were nonexistent during the summer.

The positive effect of juvenile earthworms as prey and

lack of an overwhelming negative effect of adult

earthworms through indirect effects was interesting for

two reasons: (1) juvenile earthworms (2.5 g) were only

added once at the beginning of the 20 week experiment

and (2) adult earthworms significantly reduced the

amount of leaf litter and microinvertebrates found in

enclosures over the summer. In addition, for juvenile

salamanders the ‘‘direct effect’’ of juvenile earthworms

also reduced the amount of leaf litter in enclosures. This

likely stemmed from enough juvenile earthworms

growing too large to be eaten thus escaping predation

by juvenile salamanders to significantly reduce leaf litter

and microinvertebrates in enclosures; nearly twice as

many juvenile earthworms were recovered from enclo-

FIG. 4. Amount of leaf litter remaining (mean 6 SE) in enclosures with (a) adult and (b) juvenile salamanders at the end of 20weeks over the summer. Abbreviations are: EE, ecosystem engineering effects; and IE, indirect effects. Solid symbols representdirect effects (i.e., juvenile earthworms) present, and open symbols represent no direct effects (i.e., no juvenile earthworms) present.


sures with juvenile compared to adult salamanders.

However, the significant ‘‘direct effect’’ in the GLM was

still positive for juvenile salamanders, indicating that the

amount of food provided by just a few of the juvenile

earthworms outweighed any negative indirect effects

from reductions in microinvertebrate numbers.

Over the winter, there were no significant effects of

ecosystem engineering, indirect, or direct effects on mass

change despite a likely overabundance of juvenile

earthworms as prey in the winter round of the

experiment. This was not surprising as ectothermic

salamanders reduce their feeding and other activity in

winter (Vernberg 1953, Hoff 1977). However, earth-

worm burrow presence (i.e., an ecosystem engineering

effect) increased adult survival by ;40% over the winter.

Survival for all treatments over the winter for adults was

higher than in a previous study: ;80% compared with

50% in treatments with adult earthworms, and ;50%compared to ,20% without burrows or adult earth-

worms (Ransom 2011). Adult P. cinereus are not freeze

tolerant (Storey and Storey 1992), and juveniles are

unlikely to be either. MLBS had a deep, sustained

snowpack during the winter of 2009–2010 (T. S.

Ransom, personal observation), likely providing insula-

tion and preventing freezing of the ground surface. The

relative importance of belowground habitat over the

winter appears to vary by year. Belowground habitat

creation also varied by size of salamanders. Unlike adult

survival, juvenile survival over the winter was high

regardless of the presence of burrows, at least during this

mild winter.

The differences seen in the relative effects between

seasons makes it likely that positive direct effects also

will vary with other abiotic or biotic factors that differ

between geographic areas. For example, soil pH and

Ca2þ availability can influence earthworm abundances

(e.g., Chan and Mead 2003, Reich et al. 2005). In

addition, the local presence or abundance of predators

that prey on both earthworms and salamanders could

also influence the relative importance of direct, indirect,

and ecosystem engineering effects. For instance, the

faster growth rates of earthworms compared to sala-

manders might increase apparent competition, with a

greater effect of increasing a common predator of both

salamanders and earthworms (e.g., shrews or garter

snakes). One aim of future studies might be to

investigate the effects of invasive earthworms on

abundances of common predators of earthworms and

salamanders although detecting apparent competition

on salamanders may be complicated because earthworm

burrows also serve as refuges from predators like garter

snakes (Ransom 2011).

Lumbricus terrestris is a common invasive earthworm

species in North America, but it is only a single

earthworm species in a taxon that contains numerous

ubiquitous invasives and many poorly described, locally

abundant native species throughout the range of the

widespread and ecologically important P. cinereus

(Hendrix 1995). In this study, the positive direct effects

in the summer and positive ecosystem engineering effects

in the winter eclipsed the negative indirect effects of L.

terrestris. The positive direct effect found here likely is

consistent across other earthworm species as well.

Plethodon cinereus will consume both native and

invasive earthworms as long as they are size appropriate

(T. S. Ransom, unpublished data), and invasive earth-

worms are an important component in the diets of

salamanders in New York and northern Pennsylvania

(Maerz et al. 2005). The nutritional value of earthworms

is likely not to vary greatly across species, implying that

PLATE 1. Plethodon cinereus found in an earthworm burrow (A) during a night survey on a natural forest plot and (B) in anexperimental enclosure. Photo credits: (A) Eric Liebgold, (B) Rita Caceres.


the direct effects of earthworms on P. cinereus should be

consistent among earthworm species.

However, the ecosystem engineering and indirect

effects of earthworms on P. cinereus are likely to differ

among earthworm species. Earthworms are placed in

different ecological groups based on their burrowing

and feeding ecology (Edwards and Bohlen 1996).

Lumbricus terrestris is an anecic species, building deep

(up to 2 m), vertical burrows but feeding on surface

litter. Epigeic earthworms are non-burrowing and feed

on surface organic matter (including leaf litter). Endo-

geic species create extensive branching burrows 0–50 cm

beneath the ground surface, feed on decomposed

organic matter in mineral soil, and mix organic and

surface soils. The ability of earthworms to provide an

overwintering refuge for salamanders likely varies based

on burrow size and depth. For instance, the endogeic

earthworm, Dendrobaena octaedra, is freeze tolerant and

builds shallow burrows that may not be below the frost

line within the soil (Rasmussen and Holmstrup 2002).

Differences in indirect effects likely depend upon a

combination of feeding ecology and the quality of leaf

litter in an area. Epigeic earthworms commonly are

correlated with reductions in microinvertebrate densities

(McLean and Parkinson 1998, McLean and Parkinson

2000). In New York, invasive earthworms were impli-

cated in P. cinereus declines and correlated with

reductions in leaf litter and associated microinverte-

brates (Maerz et al. 2009); the most common species in

that study area were the anecic L. terrestris and L.

rubellus, an epigeic species (Nuzzo et al. 2009), both of

which are associated with declines in leaf litter (Gundale

et al. 2005). In these field studies, the indirect effects of

L. terrestris seem more pronounced than in the current

study, where the indirect effect of L. terrestris on P.

cinereus was overshadowed by the direct effect of

earthworms as a food resource. One reason for this

discrepancy among studies may be due to the poor

quality oak leaf litter at MLBS that was used in the

enclosures (see Zicsi 1983 regarding litter palatability

and earthworms). Higher palatability of leaves could

increase the negative indirect effects of earthworms

through increased consumption of leaf litter (Suarez et

al. 2006). In fact, the data reported by Nuzzo et al.

(2009) appear to show a stronger negative correlation

between earthworm biomass and leaf litter volume in

sugar maple-dominated sites compared with oak-dom-

inated sites.

This is one of few studies to simultaneously examine

multiple interaction pathways of an ecosystem engineer

(but see Usio and Townsend 2004, Daleo et al. 2007,

Miyashita and Takada 2007). Here I was able to

measure the relative importance of ecosystem engineer-

ing, direct, and indirect effects, and was able to

demonstrate that, in this model system during the

summer, positive direct effects of L. terrestris out-

weighed the negative indirect effects through the

consumption of leaf litter; ecosystem engineering effects

increased adult survival over the winter. Plethodon

cinereus, one of the most abundant vertebrates in

eastern North American forests, is an important

component of woodland ecosystems (Mitchell et al.

1997, Davic and Welsh 2004). The direct interactions

between earthworms and P. cinereus may be an

important belowground–aboveground linkage. Below-

ground engineers, such as earthworms, often are

overlooked in examinations of species in aboveground

communities, but can be quite important, not only

through habitat modification, but as prey, predators, or

competitors (Hendrix 2006, van der Putten et al. 2009).

This study shows that it is important to examine the

multiple pathways through which an ecosystem engineer

may interact with another organism, and that the

strength of these pathways may change over time (e.g.,

between seasons or age classes).

ACKNOWLEDGMENTS

I thank Mountain Lake Biological Station for resources anduse of their property. I am grateful to A. Al-Haj, B. Billak, R.Caceres-Charneco, M. Childs, C. Espada, A. Harper, L. Kintz,E. Liebgold, D. Rearick, C. Shepard, K. Staples, E. Susko, andG. Taylor for their labor and assistance. I thank H. Wilbur, L.Avila, K. Burke, E. Liebgold, A. Moore, T. Park, S. Seamster,and R. Smith for helpful comments on an early draft of thismanuscript. Funding provided by an NSF-DDIG grant (DEB-0910074) to T. S. Ransom. McCormicke provided mustardpowder used to extract earthworms. The experiments complywith current U.S. laws, and research was approved andconducted under Virginia Department of Game and InlandFisheries scientific collection permit no. 030986 and UVAACUC protocol no. 3063 to T. S. Ransom.

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