How can a mouse be a consumer and a prey

Our findings highlight the contingent but predictable effects of locally abundant food on risk experienced by incidental prey, which can be positive or negative depending on both spatial proximity and relative preference. This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: All raw data pertaining to small mammal trapping, predator activity and space use, and consumption of incidental prey items are available from the Dryad database DOI: This grant was authored by and awarded to EMS. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist.

Predator foraging behaviors, and the resulting distribution of predation risk within a landscape, are influenced by what prey are available and where they are located. Optimal foraging theory provides a framework for predicting predator choice of prey on the basis of energetic profitability [ 1 ], as well as the spatial distribution of predator foraging efforts in relation to local prey availability [ 2 , 3 ].

Increased abundance of generalist predators, which are numerically decoupled from the abundance of some prey, can increase the likelihood of localized extinction for sparse or rare prey items [ 4 ]. These sparse or rare items are especially vulnerable when encountered and consumed opportunistically as incidental prey while predators forage for primary, or locally abundant, foods [ 5 ].

Abundant food sources can supplement predator diets [ 6 — 9 ] elevate predator densities [ 10 , 11 ], and influence generalist foraging strategies and space use [ 12 , 13 ], suggesting that the distribution of primary food resources may play a crucial role in determining local risk to incidental prey. Researchers have identified several scenarios whereby primary prey can influence the impacts of generalist predators on incidental prey.

Primary prey sources can, when abundant, reduce predation risk for incidentally encountered and less-preferred prey items [ 14 — 19 ]. Alternatively, abundant primary prey can increase local predator densities through aggregative and numerical responses [ 20 , 21 ], producing apparent competition that increases local predation rates on incidental prey that are preferred or highly vulnerable [ 22 — 24 ].

For example, deer feeders dispensing corn Zea mays spatially concentrate foraging by raccoons Procyon lotor , increasing predation risk for nearby nests of wild turkeys Meleagris gallopova and turtles [ 25 , 26 ]. On the other hand, locally abundant food also can draw predators away from opportunistically consumed prey items like waterfowl nests located in different areas [ 27 ].

These disparities in indirect effects of primary prey on incidental prey via a shared predator may be explained by the spatial scales at which predators are active and the preference ranking of available foods.

However, few investigations have attempted to quantify the spatial scale at which spatially concentrated foods influence predator activity and foraging behavior. Optimally foraging generalists should preferentially consume the most profitable prey items available [ 28 ], so the relative profitability of abundant prey will determine at least in part whether incidental prey are consumed or disregarded.

This reasoning raises a series of questions: 1 at what spatial scale do localized, abundant food sources influence predator space use and foraging behavior, 2 how do abundant food sources influence predator preference for other prey items, and 3 how does the profitability of abundant food influence consumption rates on incidental prey of differing profitability? To answer these questions, we provided abundant, localized food sources of differing profitability in order to manipulate predator space use and foraging behavior.

We then quantified both predator activity and consumption rates on two incidental prey items of differing nutritional content relative to these localized food sources. Distributed widely across North America, the white-footed mouse consumes fruits and fungi [ 29 , 31 ], and is an important predator of tree seeds [ 32 — 34 ]. White-footed mice are also noted predators of gypsy moth pupae Lymantria dispar ; [ 35 — 37 ] and songbird eggs and fledglings [ 18 , 38 — 40 ]. Abundant food sources may influence predation risk to white-footed mouse prey by concentrating mouse space use and altering mouse preference for prey items relative to what prey are available [ 34 ].

For example, highly preferred foods such as sunflower seeds Helianthus annuus may decrease predation on less-preferred incidental prey items e. In addition, a locally abundant food source may draw mice away from areas farther away from this food source, generating refugia.

Our investigation aims to quantify and compare spatial patterns of white-footed mouse foraging behavior and activity with spatial patterns of predation risk to and consumption of incidental prey.

In particular, we evaluate how localized and abundant, highly and less-preferred food resources affect and potentially generate discrepancies between patterns of mouse activity and consumption of incidental prey.

We hypothesized that mice would forage for and consume incidental prey in a manner consistent with optimal foraging theory. It follows that we should expect the presence of a more-preferred food to cause mismatches in the spatial patterns of incidental prey consumption and mouse activity, especially near the food source. Given that white-footed mice are important predators of tree seeds, we used almonds Prunus dulcis and sugar maple seeds Acer saccharum as incidental prey.

While not naturally occurring in this system, the nutritional profile of almonds by weight; Sugar maple seeds have also been demonstrated to be consumed by white-footed mice with intermediate preference relative to other prey items [ 32 , 34 ].

Abundant foods can cause consumers to become more selective, so alterations to mouse preferences for and consumption of incidental prey maple seeds may demonstrate the potential for effects on tree recruitment rates and plant diversity at scales consistent with mouse foraging [ 43 ]. In addition, these incidental prey items can be considered substitutes for other sessile prey of white-footed mice e.

We evaluate if abundant food sources influence local mouse densities, and thus mouse activity, space use, and foraging behavior. Finally, we discuss how heterogeneity in predation risk ultimately impacts the existence of refugia and the ability of incidental prey populations to exploit these areas of decreased risk.

Specifically, we tested the following a priori predictions Fig 1 :. A Predictions 1 and 2: Feeders provisioned with highly sunflower seeds and less-preferred corn food sources would concentrate mouse track activity near the feeder while simultaneously decreasing activity at intermediate distances 15 and 25m from the feeder. B Predictions 3 and 4: Mouse consumption of highly preferred incidental prey almonds would be increased around 0 and 10m , and decreased at intermediate distances 15 and 25m from, feeders provisioned with abundant, highly and less-preferred food.

C Predictions 3 and 5: Mouse consumption of less-preferred incidental prey maple seeds would be increased around 0 and 10m , and decreased at intermediate distances 15 and 25m from, feeders provisioned with abundant, but less-preferred food.

Conversely, mouse consumption of maple seeds would be decreased around feeders provisioned with highly-preferred food, but would increase with distance from the feeder. The relevant animal care protocol was 07— Land surveys found dominant overstory species included white oak Quercus alba , black oak Quercus velutina , hickory Carya spp.

Noted prominent understory species including eastern redbud Cercis canadensis , flowering dogwood Cornus florida , and rusty black-haw Viburnum rufidulum ; [ 45 ] , however non-natives including wild rose Rosa multiflora and Japanese honeysuckle Lonicera japonica have invaded the forest interior [ 46 ].

We employed a 3-treatment supplemental sunflower seeds, supplemental corn, or empty feeder control crossover design with 6 plots as experimental units. Each plot contained concentric rings with radii of 5, 10, 15, 25 and 40 m centered on a feeder 0 m , as well as 8 radial trapping transects oriented along cardinal and secondary compass directions. Each treatment was applied to a plot during a 2-week period, separated from other treatments by a 1-week recovery period.

Small mammal population densities were estimated by live-trapping at the beginning and end of the experiment. The feeder on each plot was constructed from a galvanized steel trash can L and lid. Four, 4-cm holes were drilled in the bottom of each can and 3. Empty feeders served as control treatments, whereas ad libidum sunflower seeds and cracked corn were used as supplemental food sources by weight: dried sunflower seed kernels: We predicted that sunflower seeds would be highly preferred food and cracked corn would be less-preferred based on their respective energy densities and because P.

Each plot received a separate 2-week trial for each of the 3 food treatments sunflower, corn, or empty provided in the periods of 12—23 April, 3—14 May, and 24 May—4 June. The 6 possible food trial sequences e. Food was removed at the end of each trial i. Abundant food sources can spatially concentrate predators, thereby increasing local predator densities and foraging efforts.

We used trapping webs [ 48 ] to estimate pre- and post-experiment mouse densities. Sherman Traps, Inc. Each pair of traps was covered with a wood board to provide shelter against environmental conditions. Traps on all plots were baited with oats, provisioned with cotton bedding, and opened at ca. Traps were checked and closed the following mornings at ca.

Each captured animal was marked with a Monel ear tag in each ear, examined to determine sex, reproductive condition, and age, then immediately released. Traps were not set or baited during the period when supplemental food or incidental prey were deployed. Mouse activity was quantified using track plates, consisting of graphite-coated acetate sheets affixed to aluminum flashing [ 49 , 50 ]. Rings at distances of 0, 5, 10, 15, 25 and 40 m received 4, 4, 8, 12, 20, and 32 track plates uniformly spaced, respectively, for a total of 80 track plates per plot.

Track plates were monitored 4—5 times in each 2-week feeding trial at intervals of 1, 2, or 4 days depending on day of plate deployment and accounting for weekends.

All plates were closely inspected for the presence of tracks and, if present, tracks were identified to species. Our incidental prey items almonds and sugar maple seeds were prepared for field deployment by embedding them in unscented beeswax Strahl and Pitsch Inc. This method of preparation required predators to expend some effort in consuming the prey items and to leave marks that could be used to identify the predator responsible for the depredation event.

Burlap was cut into 4- x 4-cm squares and then double coated with beeswax. Short 1. A whole almond was placed inside a mold on a pre-waxed burlap square, and the mold was filled with molten beeswax until most of the almond was encased by wax. The wax was allowed to cool and the PVC mold was removed, leaving the almond affixed to the burlap. Maple seeds were affixed individually to burlap by spooning molten wax over the seed wing.

All prey items were handled with latex gloves for the entirety of their preparation and deployment. The schedule for incidental prey deployment was the same as that for food treatments and track plates. Rings at distances of 0, 5, 10, 15, 25, and 40 m received 4, 4, 8, 8, 12, and 12 of each incidental prey item, respectively, for a total of 96 prey items per plot. We deployed incidental prey items at random compass bearings within each ring, staking each into the ground using a bamboo skewer, and monitored them every 1, 2, or 4 days same as for track plates for each 2-week food trial.

The presence or absence of each prey item was noted and, if depredated, the item was closely inspected for tooth-marks, pattern of damage, and the presence of scat. Consumption events were typically attributed to mice or raccoons based on tooth-marks or scat. If the item was present and intact, it was left in place.

Each depredated item was replaced with a new prey item at a new random bearing within the same ring to avoid predators learning to return to sites of previous encounters. Live-trapping data from each trapping session and plot were analyzed using program DISTANCE to estimate mouse densities [ 48 ] before and after the experiment.

We used program DISTANCE to evaluate a variety of detectability functions created using all possible combinations of key functions half-normal, uniform, and hazard rate and adjustment factors cosine, simple polynomial, and hermite polynomial. We used a paired t-test to test whether model-averaged estimates of mouse density differed between pre- and post-experiment periods.

Plot was the experimental subject with random intercept, to account for non-independence of data from each plot, and food treatment, distance from the feeder, interval since the last check 1, 2, or 4 days , sampling period first, second, or third , and the interaction of distance and food treatment were used as categorical explanatory variables. We tested for an interaction of distance and food treatment based on our predictions that different food treatments would produce different patterns of track activity or prey consumption at varying distances from the feeder.

All raw data pertaining to small mammal trapping, predator activity and space use, and consumption of incidental prey items have been deposited at Dryad, DOI: We captured mice a total of times over 10 trap nights.

Our trapping web data lent the most support to a half-normal, cosine detectability function from both pre- and post-experiment trapping sessions, but considerable support remained for 2 alternative functions in each period Table 1. Model-averaged estimates of pre-experiment densities ranged from 1. Remember that most animals eat more than one kind of food. The students will begin to see how complex a food web is. Next add the secondary and tertiary consumers in rows above the producers.

Again, discuss the connections between primary, secondary, and tertiary consumers. Next add the scavengers: hyenas can be predators as well as scavengers and vultures. Finally, discuss decomposers—bacteria, fungi and worms that feed on the decaying matter—and their role in the food web. Students should now have a complete understanding of the complexity of the food web.

At right is an example of a food web. All living things need energy to stay alive. This energy comes from the sun. Plants make their food from energy from the sun. Animals get their energy from the food they eat. Animals depend on other living things for food. Some animals eat plants while others eat other animals. This passing of energy from the sun to plants to animals to other animals is called a food chain.

Ask students to name all the different animals that are dependent on the one tree. First demonstrate a food chain, a simple interdependence , by linking the student with the sun card the source of all energy to the student with the grass card to the student with the zebra card to the student with the lion card.

Balance is key! Explain that the interactions in a grasslands system are more complicated than this. Have the participants now stand in a circle, out of order i. Give the ball of string to the person with the sun. Then ask that person to pass the yarn to the person with a card of an organism that the sun supports. If the sun supports more than one organism in the circle, pass the string back to the sun and from the sun to the other organism that it supports.

Keep going through the chain until you get to the top consumers. The string will be a tangled web in the middle of the circle. Food chains are complicated, and the balance they create is essential. For example, the impact of overhunting will cause the lions to drop their strings. What happens? This activity requires a large open area. In a class of 25 to 40 students, choose three to five to be predators and seven to ten to be plant-eaters. The remainder will be plants.

This represents a balanced system where plants are more plentiful than plant-eaters, plant-eaters more plentiful than predators, and predators are the least plentiful. The students can select which plant-eaters and predators will be in their groups. Each group selects hand-signals that will differentiate them from the other groups.

Example: the plants may want to hold their hands out to their sides to represent leaves, the plant-eaters oryx may hold their hands on the heads to represent horns, and the predators lions may hold their hands up like paws with the claws showing. The predators try to tag the plant-eaters who try to tag the plants. Since predators decompose when they die and become fertilizer, the plants try to tag the predators. Once you are tagged, you turn into whatever tagged you. After a period of time, stop the game to see how many plants, plant-eaters, and predators are left.

Play should resume but should be stopped a few times before the end to determine what has happened and why. After playing a few rounds of the game, select one of the plants to re-enter the game as a human. The rules for the human are different: the human can tag anyone, but no one can tag the human.

Each time the human tags someone, that player becomes another human. See how long it takes before all players have become changed into humans.

For example, grass in a forest clearing produces its own food through photosynthesis. A rabbit eats the grass. A fox eats the rabbit. When the fox dies, decomposers such as worms and mushrooms break down its body, returning it to the soil where it provides nutrients for plants like grass.

This short food chain is one part of the forest's food web. Another food chain in the same ecosystem might involve completely different organisms.

A caterpillar may eat the leaves of a tree in the forest. A bird such as a sparrow may eat the caterpillar. A snake may then prey on the sparrow. An eagle, an apex predator , may prey on the snake. Yet another bird, a vulture, consumes the body of the dead eagle.

Finally, bacteria in the soil decompose the remains. Algae and plankton are the main producers in marine ecosystems. Tiny shrimp called krill eat the microscopic plankton. The largest animal on Earth, the blue whale, preys on thousands of tons of krill every day. Apex predators such as orcas prey on blue whales.

As the bodies of large animals such as whales sink to the seafloor, detritivores such as worms break down the material. The nutrients released by the decaying flesh provide chemicals for algae and plankton to start a new series of food chains.

Biomass Food webs are defined by their biomass. Biomass is the energy in living organisms. Autotrophs, the producers in a food web, convert the sun's energy into biomass. Biomass decreases with each trophic level. There is always more biomass in lower trophic levels than in higher ones.

Because biomass decreases with each trophic level, there are always more autotrophs than herbivores in a healthy food web. There are more herbivores than carnivores. An ecosystem cannot support a large number of omnivores without supporting an even larger number of herbivores, and an even larger number of autotrophs.

A healthy food web has an abundance of autotrophs, many herbivores, and relatively few carnivores and omnivores. This balance helps the ecosystem maintain and recycle biomass. Every link in a food web is connected to at least two others. The biomass of an ecosystem depends on how balanced and connected its food web is. When one link in the food web is threatened, some or all of the links are weakened or stressed. The ecosystems biomass declines. The loss of plant life usually leads to a decline in the herbivore population, for instance.

Plant life can decline due to drought , disease, or human activity. Forests are cut down to provide lumber for construction. Grasslands are paved over for shopping malls or parking lots.

The loss of biomass on the second or third trophic level can also put a food web out of balance. Consider what may happen if a salmon run is diverted. A salmon run is a river where salmon swim.

Salmon runs can be diverted by landslides and earthquakes, as well as the construction of dams and levees. Biomass is lost as salmon are cut out of the rivers. Unable to eat salmon, omnivores like bears are forced to rely more heavily on other food sources, such as ants. The area's ant population shrinks. Ants are usually scavengers and detritivores, so fewer nutrients are broken down in the soil. The soil is unable to support as many autotrophs, so biomass is lost. Salmon themselves are predators of insect larvae and smaller fish.

Without salmon to keep their population in check, aquatic insects may devastate local plant communities. Fewer plants survive , and biomass is lost. A loss of organisms on higher trophic levels, such as carnivores, can also disrupt a food chain. In kelp forests , sea urchins are the primary consumer of kelp. Sea otters prey on urchins. If the sea otter population shrinks due to disease or hunting, urchins devastate the kelp forest.

Lacking a community of producers, biomass plummets. The entire kelp forest disappears. Such areas are called urchin barrens. Human activity can reduce the number of predators. In , officials in Venezuela dammed the Caroni River, creating an enormous lake about twice the size of Rhode Island. Hundreds of hilltops turned into islands in this lake. As a result, prey animals like howler monkeys, leaf-cutter ants, and iguanas flourished. The ants became so numerous that they destroyed the rainforest , killing all the trees and other plants.

The food web surrounding the Caroni River was destroyed. Bioaccumulation Biomass declines as you move up through the trophic levels.

However, some types of materials, especially toxic chemicals, increase with each trophic level in the food web. These chemicals usually collect in the fat of animals. When a carnivore eats several of these herbivores, it takes in the pesticide chemicals stored in its prey. This process is called bioaccumulation. Bioaccumulation happens in aquatic ecosystems too. Runoff from urban areas or farms can be full of pollutants.

Tiny producers such as algae, bacteria, and seagrass absorb minute amounts of these pollutants. Primary consumers, such as sea turtles and fish, eat the seagrass. They use the energy and nutrients provided by the plants, but store the chemicals in their fatty tissue. Predators on the third trophic level, such as sharks or tuna, eat the fish.

By the time the tuna is consumed by people, it may be storing a remarkable amount of bioaccumulated toxins. Because of bioaccumulation, organisms in some polluted ecosystems are unsafe to eat and not allowed to be harvested.