Arthropod Corpses in a Temperate Grassland: A Limited Supply?

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Arthropod Corpses in a Temperate Grassland: A Limited Supply?Author(s): J. Retana, X. Cerdà and X. EspadalerSource: Holarctic Ecology, Vol. 14, No. 1 (Jan., 1991), pp. 63-67Published by: Wiley on behalf of Nordic Society OikosStable URL: http://www.jstor.org/stable/3682187 .

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HOLARCTIC ECOLOGY 14: 63-67. Copenhagen 1991

Arthropod corpses in a temperate grassland: a limited supply?

J. Retana, X. Cerda and X. Espadaler

Retana, J., Cerda, X. and Espadaler, X. 1991. Arthropod corpses in a temperate grassland: a limited supply? - Holarct. Ecol. 14: 63-67.

The disappearance of arthropod corpses in a temperate grassland of the Mediterrane- an coast (Barcelona, Spain) has been analyzed in this study. The mean time in which the corpses stayed out in the field is less than five minutes (x = 285 + 282 s), in a range of 2-2228 s. This holds true in cleared areas as well as in high vegetation areas. Ants are the principal scavengers of this type of remains, although the species that collect them vary according to the time of day and season of year, with the corpses' disappearance being the most rapid during the middle hours of the day, precisely when ants' density on the ground is less. The reason for this was the peak daytime abundance of insectivore, opportunistics ants. Anyway, the short time lapse that the prey stay in the field - at any time of the day - can be considered as an indirect estimate of the scarcity of these resources.

J. Retana, CREAF, Autonomous Univ. of Barcelona, E-08193 Bellaterra, Spain. - X.

Cerdd, CID, CSIC, c/Jorge Girona 18-26, E-08034 Barcelona, Spain. - X. Espadaler, Dept of Animal Biology, Vegetal Biology and Ecology, Autonomous Univ. of Barce- lona, E-08193 Bellaterra, Spain.

Introduction

In the analysis of the structure and relationships in animal communities, food is considered as a limited resource for which an intense rivalry is established (Schoener 1974). The majority of studies that deal with this theme in ants (Brown and Davidson 1977, Bern- stein 1979, Briese and Macauley 1980, Nielsen 1981, Klotz 1984, Delalande 1986) understand, a posteriori, that the different use of time by the species that are present in a specific biotope precludes this rivalry. Ob- viously, this is not the only possible interpretation of the structure of animal communities and, in fact, the role of predation is receiving increasingly greater attention (Holt 1984, Begon et al. 1987). In the specific case of ants it is known that they are preyed upon by a multi- tude of animals: spiders (Mackay 1982), reptiles (Whit- ford and Bryant 1979), amphibians (Lizana et al. 1986), birds (Herrera 1983), etc., and there has been a recent proposal by Hunt (1983) which suggests the influence of predators in their morphology and food-gathering strategies. In any case, and without forgetting other possible

explanations, succession in time of species reduces aggressive behavior and allows for a more efficient exploitation of the resources. This makes the coexistence of a greater number of species possible (Briese and Macau- ley 1980, Baroni Urbani and Aktaq 1981, Delalande 1986).

It is necessary to confirm that the period of resource availability in the field is low to be able to accept that species that are active at a specific time of the day do, in fact, exploit the nutrient resources that are inaccessible to competitors who have a different activity rate. An ultimate interpretation is not able to be contrasted ex- perimentally, but the eventual food scarcity is more or less directly measurable, and, thus, it is relevant. Some of the resources that might be limited, such as molasses or seeds, are measurable to a certain extent, since it is possible to estimate their distribution and abundance within certain limits. This is not the case with insect cadavers since these are unpredictably distributed in time and space, and until now valid methods for quanti- fying their availability at all times have not been devel- oped.

Accepted 16 February 1990

( HOLARCTIC ECOLOGY

HOLARCTIC ECOLOGY 14:1 (1991) 63



Tab. 1. Mean time (s) (? SD) and scavenging range of the insect corpses placed in the field on the various days of meas- urement (n is the number of observations).

Day n Mean time Range (s) ? SD

11 May 1986 89 309?387 5-1740 27 May 1987 198 380?345 2-2058 14 Jun 1986 110 276?263 3-1205 5 Jul 1986 145 172?191 2-975

28 Jul 1987 262 287?285 2-2228 31 Jul 1986 95 227?215 10-2042 3 Sep 1986 117 257?279 2-1240

30 Oct 1986 32 480?259 60-1320

Total 285?282 2-2228

In spite of the fact that invertebrates represent a high proportion of the animal biomass, information that ex- ists on the degradation process of their cadavers in the field, as well as those organisms implicated in this process, is scarce. There are exact data on the disappearance and consumption of insect cadavers that are of a small size such as moths and flies (Fellers and Fellers 1982) or wasp larvae (Jeanne 1979), and also of others of greater size such as crickets (Seastedt et al. 1981). However, there are many factors that can condition the results that are obtained - hour of the day, season of the

year, latitude, biotope characteristics, the method used, etc. Thus, a greater number of studies in this sense can

clarify ideas on the use of these nutrient resources in animal communities.

This study analyzes the disappearance of insect cadavers in the savanna-like meadow of the Mediterrane- an region. Considerable previous work has been done there in relation to the activity of feeding of the principal ant species that inhabit it (Bosch et al. 1987, Cerdai et al. 1988, Retana et al. 1988). For this reason, it is an

appropriate site in which to develop a study of this type.

Material and methods

This study was carried out in Canet de Mar (Barcelona), Spain, for eight days of observation, from the months of

May, 1986, to October, 1987. Each day, from one to three observers would place bait in the field from the

early morning to the late afternoon. The bait which was offered arthropod cadavers that had previously been

captured in the same area and killed there, and whose size (2-8 mm) made it possible for the ants to gather them individually.

The observations were made from two different mi- crohabitats: 1) In cleared areas and in roads, remains were distributed in a provisional fashion and were inspected and checked by an observer from a distance of 1-1.5 m. Their placement was continually varied to prevent memorization of their location by the worker ants.

Elapsed time was measured from the moment in which

the baits were situated in the field until they were found by the animal which wound up carrying them off, in each case noting the time taken and the species that gathered them. In total, 1061 observations were carried out. 2) Parallel to these observations, others in higher vegetation zones were carried out to test the disappearance of remains under these conditions. To do this, 20 baits on portions of white plastic were distributed in the grass. For one hour, and in 12 observations - separated by five minutes each - the number of baits that still remained in their original places was checked. This was repeated ten times a day, yielding a daily total of 200 inspections.

The ant density on the ground surface was deter- mined by placing a total of six 1 m2 frames in which every two hours the number of worker ants of each species was counted. The total values for each hour and for each species were obtained by adding up the values obtained in all frames.

Results

Of the 1061 baits which were placed in the field, 1029 (97%) were gathered up in <40 min, all being gathered by ants. Alltogether, the mean time in which the cadavers stayed in the field was very short, <5 min (X = 285 s), although the time varied considerably, in a range of from 2 to 2228 s (Tab. 1).

In Fig. 1, the percentage of baits that remained uncollected during successive periods of time beginning with their placement in cleared areas and vegetation in one of the study days (3 Sep 1986) is represented. The curves for the vegetation and cleared areas are similar, with a rapid disappearance of prey in the first few minutes after being placed; the curves are distinguishable only in one aspect: the percentage of uncollected items in vegetation is higher than that of the cleared areas.

The speed of the corpses' disappearance varies throughout the day. As an example (Tab. 2), the results of 14 Jun 1986 are grouped in three periods, separated according to the total ant density on the ground and the dominant species at each moment. Contrary to expecta-

% ITEMS

100

80

40

20- o- --. .... - -e

10 20 30 40 50 60

TIME (MIN)

Fig. 1. Curves of corpse disappearance in the cleared areas (solid line; n = 117), and in vegetation (broken line; n = 200) on 3 Sep 1986.

64 HOLARCTIC ECOLOGY 14:1 (1991)



Tab. 2. Percentage of corpses that remained in cleared areas after 1, 5, 10, 15 and 20 min from the time of being placed on the ground, at three different times of the day on 14 Jun (solar time). The total number of prey offered (PO) and the total ant density (ants m-2) are indicated.

% corpses that remain after

Hours ants m-2 PO 1 min 5 min 10 min 15 min 20 min

6-8 16.7 30 86.7 53.3 26.7 10 0 9-13 3.3 33 63.6 18.2 6.1 0 0

14-19 11.5 47 91.5 40.4 4.3 0 0

Total 110 81.8 37.3 10.9 2.7 0

tion, the baits' disappearance is more rapid in the middle hours of the day, precisely when the ant density is lower. This is due to the fact that during these hours the dominant ants are primarily insectivore and opportunistic species such as Aphaenogaster senilis and Cataglyphis cursor which, despite their low density on the ground, perform a very efficient sweep of arthropod remains.

The different degree of efficiency of the ant species of the area is clearly shown in Tab. 3, where the abundance of each species in the frames and the percentage of collected items by each species at different hours of 28 Jul 1987 are indicated. The ants that largely chose to gather the baits were A. senilis in the morning and in the mid-afternoon; C. cursor at midday; and Pheidole pallidula at dusk. This does not quite correspond with the abundance values in frames, since within these a considerable number of ants that collected very few items, such as Camponotus foreli, an essentially nectarivorous species, and two species of the genus Messor, essentially granivorous are found. The baits disappeared in all seasons in a relatively short period of time (see Tab. 1), but in each season, the species that used them were different, in accordance with their abundance. Other

ants, such as Tapinoma nigerrimum and Tetramorium semilaeve, gathered few baits on the day described due to their relative scarcity in the field in this season. But they can be, and in fact on other days were, important competitors to the previously mentioned species for arthropod remains.

Discussion

The principal result of this study is the rapid disappearance speed of arthropod cadavers in the area that was studied: the mean time in which the cadavers stayed out was 4.75 min, with almost 97% of the baits found in <40 min. These data, which refer to a cleared area with an abundance of all types of insects, agree with the scarce data that exist on the survival rate of animal remains in the fields. In a similar study performed in a Maryland oak forest, Fellers and Fellers (1982) found that all remains were gathered up in less than 36 min, with a mean time of 6.75 min. Other studies that do not directly refer to this theme also contribute similar data: in a study on habitat exploitation in Cataglyphis cursor, Querard (1985) verified that the time taken to discover

Tab. 3. Relative abundance (Ab) of each ant species in the frames placed in cleared areas and the percentage of item that it collects (Coll) at different times of the day on 28 Jul 1987 (solar time). The total ant density (ants m-2) and the number of preys offered (PO) each hour are indicated.

Hour ants PO Tapinoma Aphaenogas- Pheidole Cataglyphis Camponotus Messor Messor Tetramorium m-2 nigerrimum ter senilis pallidula cursor foreli bouvieri capitatus semilaeve

% % % % % % % % % % % % % % % % Ab Coll Ab Coll Ab Coll Ab Coll Ab Coll Ab Coll Ab Coll Ab Coll

6 15.7 5 1 0 11 100 16 0 0 0 3 0 44 0 20 0 5 0 7 17 0 18 59 23 0 0 0 0 8 4.5 25 0 0 19 40 4 0 19 52 22 0 32 0 0 0 4 0 9 18 0 28 0 61 0 0 0 0

10 1.2 37 0 0 0 0 0 0 78 100 22 0 0 0 0 0 0 0 11 20 0 0 0 100 0 0 0 0 12 0.7 10 0 0 0 0 0 0 100 100 0 0 0 0 0 0 0 0 13 31 0 10 0 90 0 0 0 0 14 2.3 33 0 3 14 40 0 6 36 46 50 0 0 0 0 0 0 0 15 25 0 80 0 8 0 8 0 0 16 10.8 10 3 0 6 80 11 0 3 0 8 10 60 0 9 0 0 0 17 19 5 11 68 0 0 5 0 11 18 5.5 12 6 0 0 0 49 83 0 0 6 0 21 0 0 0 18 17

Total 262 2 0.8 8.6 26.3 16 13.4 9.4 53.4 10.2 0.4 39.3 1.4 10.2 0 4.9 1.5

5 HOLARCTIC ECOLOGY 14:1 (1991) 65



placed baits in the the center of frames by the worker ants could vary from a few seconds to several hours; Baroni Urbani and Kannowski (1974) also verified that baits which they placed in a Lousiana meadow were found in a mean time of some five minutes, in the morning as well as in the afternoon, although in each case the species that found them were different; in a Georgia oak-hickory forest, Seastedt et al. (1981) observed that cricket corpses were found and carried off by wasps and ants a few minutes after being placed on the ground and that, in spite of being protected by bags, none were left 24 h after being placed.

The disappearance of baits in cleared areas and in areas of higher vegetation follows a log-linear model in both cases with the rapid disappearance of the greater part of the baits and the remaining of only a few for a longer period of time. These curves are similar to those that Jeanne (1979) obtained in different habitats of America, although in this case the disappearance of the baits was much slower, being measured in days and not in minutes. Jeanne (1979) found that the baits disappeared much earlier in cleared zones than in areas that had abundant vegetation. This can be related to the greater ease for discovering remains in the cleared zones and also to the greater accessibility to the remains for scavengers.

Another feature that stands out in this study is the exclusive exploitation of the remains by the ants. This predominance of ants as the principal gatherers of animal remains has also been shown in other cases: Fellers and Fellers (1982) found that all of the insect cadavers that they placed on the ground were gathered by ants; Jeanne (1979) also observed that at least 59% of the predators of wasp larvae that he placed in the field were ants; likewise, of the species that were found by Baroni Urbani and Aktaq (1981) in baits that were placed in the desert of Anatolia, only 0.06% of the predators were not ants; Seastedt et al. (1981) analyzed the invertebrate succession with cricket cadavers that were placed in the field and observed that ants were one of the

principal groups in the first succession stages, and that

they could frequently entirely consume the remains.

According to Fellers and Fellers (1982), the fact that the baits were exclusively found by ants can be due to three reasons: 1) their scavenging method is more efficient in

searching for dead insects on the ground; 2) they have a numerical advantage (ants are the dominant macro-

arthropod group in many ecosystems, Petal et al. 1971, Petal 1978, Wilson 1987); 3) the role of some vertebrates (birds, lizards, squirrels) and invertebrates (spiders, wasps, Carabidae) that are more sensitive to the presence of an observer, has been underestimated. This last hypothesis seems to have little importance in Canet de Mar, at least in the case of the remaining invertebrate groups, since representatives of these groups that are little affected by human presence appear upon other baits (as honey or cheese) during prolonged periods of time (pers. obs.). Regarding the vertebrates,

however, the picture is not clear since their importance does not seem to be very great: in inspections of baits in vegetation, one was able to see a small lizard escaping on infrequent occasions; excrement also was left behind by these reptiles on the plates in which the baits were placed. More information is needed on this aspect.

One more feature that should be taken into account is that the results obtained with small items cannot be generalized to larger ones. The size of the items that were offered in this case made it possible for individual ants to carry them to the nest. However, in the case of the larger remains, the ants that found them could not always exploit them and the remains wound up being monopolized first by other ants, normally small species that follow a method of mass recruitment that leads a large number of worker ants to the bait (H611dobler et al. 1978, Traniello 1983), and then by other arthropods, such as Diptera, Collembola and mites (Seastedt et al. 1981).

The corpses' disappearance is most rapid in the middle hours of the day, contrary to what would be expected since worker ant density is less. At this moment, the most abundant ant outside - and almost the only one - is Cataglyphis cursor. This is a thermophilic and zoonecrophagous species that individually gathers up and performs an efficient and complete sweep of insect corpses (Cerdai et al. 1990) since it has a high tempo. This allows the most ample areas of the habitat to be covered, facilitating the early discovery of food (Leo- nard and Herbers 1986). This is also characteristic of other species of arid zones that are similarly rapid (Harkness and Wehner 1977, Marsh 1985). During the rest of the day, the species that appear are more numer- ous and vary according to the seasons of the year, with opportunistic ants such as Aphaenogaster senilis, which find a large quantity of cadavers despite their presence in the field (see Tab. 3), and the other smaller, more aggressive species such as Tapinoma nigerrimum and Pheidole pallidula, which take longer to find the remains but, when once located, wind up dominating them in a short period of time by recruiting many work- ers to them.

In any case, the disappearance of the remains is almost instantaneous at any time of day. It has always been accepted that the exposure of baits in the field is very short in tropical zones (Carrol and Janzen 1973, Jeanne 1979), which is to be expected since those ecosystems are permanently active, but the results of this study and of Fellers and Fellers (1982) prove that it is similar in temperate zones. Although, this does not directly imply competition for food, the demonstration of the short time lapse that the insect cadavers stayed available can be interpreted as an indirect estimate of the scarcity of such resources. An alternate hypothesis could be based upon the ants' storage capacity: although not being used immediately, the collected items could be conserved in the nest for later consumption. A massive and continued innundation of prey would be

66 HOLARCTIC ECOLOGY 14:1 (1991)



necessary to distinguish between these alternatives ac-

cording to whether there was a saturation in their collection or not.

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Arthropod Corpses in a Temperate Grassland: A Limited Supply?