Acra Oecologica
19 (5) (1998)
425-438
/ 0 Elsevier,
Paris
Changes in the structure of dung insect communities after ivermectin usage in a grassland ecosystem. I. Impact of ivermectin under drought conditions Kerstin Kruger *$ , Clarke H. Scholtz Department of Zoology * Corresponding Received
and Entomology, University of Pretoria, Pretoria 0002, South Africa. author to: (fax: +27 12 329 3278; e-mail: n’
[email protected])
January
28, 1997;
revised
April
15, 1998;
accepted
April
28, 1998
Abstract - Changes
in structure of dung insect communities after treatment of cattle with a single standard injection of ivermectin (200 pg.kg-‘) were investigated in a large-scale field study under extensive farming conditions in South Africa. The study was carried out during a period of drought. Two herds of cattle were treated with ivermectin, whereas a further two herds remained untreated and served as controls. The four herds were kept in four paddocks of about 80 ha. Dung insect communities were monitored before and for three months after treatment. A range of community measures, including univariate, graphical and multivariate methods, were used to assess the effects of ivermectin. The results suggest that the use of ivermectin affected community structure through reduction in species diversity and an increase in species dominance. These effects appear to have lasted for three months after ivermectin treatment when experiments were terminated. 0 Elsevier, Paris
Avermectins I ecotoxicology I non-target organisms / dung beetles / climate I South Africa
1. INTRODUCTION Ivermectin belongs to the relatively recently discovered family of avermectins, which are highly potent broad-spectrum antiparasitics routinely administered to livestock [8]. With the increasing use of avermectins and with growing environmental awareness, these broad-spectrum parasiticides have become the subject of a debate in recent years concerning their environmental safety (e.g. [18, 23, 671). Avermectins have come under scrutiny because most of the administered parasiticide is ultimately eliminated via the dung where it continues to have a powerful insecticidal effect [54]. The residues in dung not only affect economically important pest species (e.g. [27, 37, 38]), but also a number of non-target organisms such as beneficial dung-breeding beetles. The literature on the impact of avermectins on dung insects has been extensively reviewed by Strong and Brown [55], Strong [53, 541, Herd [ 171 and Wratten and Forbes [65]. The chemical and pharmacokinetic properties and the mode of action of avermectins have been described by Campbell [8] and Steel [52]. Studies at the single-species level in the laboratory have revealed that ivermectin can have lethal and sublethal effects on dung-breeding insects. The latter p Present
address:
ARC-Plant
Protection
Research
Institute,
Private
manifest themselves, for example, in sterility and diminished rates of reproduction and prolonged development (e.g. [53, 541). Several field studies have been conducted to assess the effect of ivermectin on attraction of dung beetles to dung from treated animals, pat colonization and dung decomposition, and to determine the concentration of ivermectin in dung after treatment of cattle (e.g. [3, 22, 33, 34, 36, 47-5 1, 56, 60, 661). These studies have shown that geographical location and climate can influence results; for example, ambient temperature and rainfall can affect the composition of dung fauna in general (and dung insects in particular) and the rate of dung pat decomposition. However, these field studies have provided only limited insight into the extent to which ivermectin treatment affects natural populations and communities. Consequently, the need for studies to examine the ecological effects of avermectins on communities of pastureland invertebrates has been stressed by Herd et al. [19]. Moreover, most of the longer-term field investigations carried out to date were conducted in the temperate zone of the northern hemisphere, where earthworms play a major role in the degradation of dung, in contrast to Mediterranean and subtropical cli-
Bag X134,
Pretoria
0001,
South
Africa
426
K. Kriiger,
mates, where dung beetles are of greater importance 116, 20, 321. The grassland biome in southern Africa is largely restricted to the highveld plateau of the Free State province. Dung insect dynamics in this area, as in most parts of the Afrotropical Region, are greatly influenced by climatic conditions, and the amount of rainfall received during the austral summer (i.e. the rainy season) emerges as one of the major factors [lo]. Similarly, the breeding success of dung beetles and the survival of their immature stages have been shown to be reduced during times of drought (e.g. Onthophagus grandam Boheman [57]). As southern Africa is regularly subjected to periods of drought [58, 591, drought can be considered an intrinsic characteristic of the system. In the present study, the ecotoxicological effects of ivermectin on dung insect communities were assessed in a large-scale field investigation under drought conditions. The objectives of the study were: i) to determine if a single standard injection of ivermectin has an impact on dung insect communities under normal extensive farming conditions in South Africa; ii) to examine potential depressive longer-term effects of ivermectin on the communities, should such an impact occur; and iii) to determine whether the system is able to recover within a reasonable time scale, should there be a disturbance.
Scholtz
extended over three months from December 1992 to March 1993. A breeding herd of commercial cattle consisting of 80 cows, some with calves, was divided randomly into four equal-sized groups and confined to two pairs of adjacent paddocks of about 80 ha each. The two pairs of paddocks were about 200 m apart; their position is shown in figure 1. The pairs of adjacent paddocks were randomly allocated to treatment or control. The paddocks designated Pl and P2 served as control paddocks (C), and the remaining paddocks, P3 and P4, as treatment paddocks (I). The reason for allocating adjoining paddocks to each group was that cattle confined to a relatively large area were treated to reduce the effect of immigration of insects from surrounding paddocks. Although the trial paddocks were surrounded by paddocks which were also stocked with cattle, these animals rarely stayed in close vicinity to the trial area and therefore could be expected to have only minor influence on the dung insect fauna in the trial area regardless of their treatment history.
_ P2 (C) ;
PI(C) : P3(I)
2. METHODS
N : PqI)
2.1. Study site
33t,
The study was carried out in the summer rainfall region of South Africa on two virtually adjacent commercial beef-cattle farms under the same management (Farms Abel and Middelpunt, 26”54’ S, 27”35’ E). The farms are situated about 14 km east of Parys (Free State), about 1 350 m above sea level. The study site lies in the grassland biome [43] and was classified by Acocks [I] as Bankenveld, a false grassland type. The soil type is variable but is dominated by clay-loam. The paddocks were similar with regard to vegetation and the amount of rainfall received. 2.2. Meteorological
measurements
Temperature and precipitation were recorded at the nearest meteorological stations of the South African Weather Bureau at Potchefstroom and Parys, respectively. 2.3. Allocation
C.H.
and treatment
of cattle
The trial was conducted during the austral summer, coinciding with the peak beetle activity period, and
250 m
Figure 1. Position of the treatment (I) and control paddocks (C). Surrounding areas were also occupied by cattle. Treatment of entire herds with a single subcutaneous injection of ivermectin (200 ug.kg-‘) was carried out in paddocks P3 and P4. Herds in paddocks Pl and P2 were untreated (controls). Solid lines denote fences and dotted lines the line transects of artificial standardized pats placed before, and one, two and three months after treatment of cattle.
Cattle were maintained according to normal farm policy with respect to grazing and pasture management. The cattle in the treatment paddocks were treated with a single standard injection of ivermectin (200 pgekg-‘) according to the manufacturer’s recommendations; those in the other paddocks served as controls and remained untreated. A single standard injection was chosen because this is the treatment regime generally adopted in South Africa, instead of three injections per year as is customary in Europe, due to different parasite loads. Intraruminal slowrelease devices were not commercially available in South Africa until 1997. Acta
Oecologicc~
Ivermectin and dung insect community structure. I
It was not possible for logistical reasons to replicate the experiment in the same year and so replication was planned for the subsequent year. However, the experiment could not be adequately repeated as intended because the higher rainfall experienced during the rainy season of 1993/94 affected the abundance of dung insects, so that a comparison of the two years is rather complex. The results of this second study therefore is reported in a separate article [29]. 2.4. Sampling procedures Insects were collected in dung pats as opposed to dung-baited pitfall traps because pats reflect a more natural situation and allow for species interactions [21]. The colonization of pats by dung beetles and other dung insects is influenced by such dung characteristics as pat size, moisture content and nutritional properties [2, 4, 7, 401. Therefore, two types of pats were used in the trials. Artificial 1 kg pats, standardized to limit the number of factors potentially responsible for differences between the dung insect fauna in the various paddocks and made from thoroughly mixed dung from an untreated herd held at the University of Pretoria’s experimental farm, served to provide quantitative data. Cattle at the experimental farm were maintained on hay and luceme, water was available ad libitum. Dung was collected approximately one week before field sampling days and kept frozen up to one day before use, when it was defrosted. Secondly, fresh naturally-voided pats from treated and untreated animals were marked and sampled in the trial paddocks to confirm that the artificial pats provided a representative sample of the resident dung insect community and to evaluate any direct effects of ivermectin on the dung fauna. One day before treatment of cattle, 10 artificial standardized pats were placed out and labelled at 50-pace intervals in a line transect (length: 450 m) across each paddock shortly after dawn. After 24 h, the pats and 50 mm of underlying soil were dug up and placed individually in Berlese-type extractors in a greenhouse. After treatment of cattle, sampling of pats was carried out at monthly intervals for three months. For this, 10 artificial control pats of the type described above were placed in a transect in each paddock. In addition, 10 fresh, naturally-voided pats were selected randomly and labelled in each paddock. All pats and 50 mm of underlying soil were collected after 24 h and placed in the extractors in a greenhouse. Insects were extracted, identified to species level, where possible, and enumerated. Carabidae, Hydrophilidae and Scarabaeoidea were identified with the assistance of Dr S. EndrodyYounga (Transvaal Museum, Pretoria) and Staphylinidae with help from Dr M. Uhlig (Zoologisches Museum der Humboldt-Universitat, Berlin). Samples Vol. 19 (5) 1998
427 remained in the Berlese-type extractors for 14 to 21 days to allow for larval development in case of Scarabaeidae and pupal development in case of Diptera because they have a shorter generation time. The term ‘Diptera species’ refers to morphologically different kinds of pupae extracted. Voucher specimens were deposited in the Transvaal Museum, Pretoria, South Africa. 2.5. Data analysis Overall diversity was compared using species richness (S) and the Shannon index (H’; based on the natural logarithm) [35]. Although the interpretation of diversity indices has many limitations, they are still of importance for environmental impact studies [ 141. The Shannon index has the advantage that significant differences between two samples can be assessed by calculating a t-value using the method developed especially for this index by Hutcheson [25]. The evenness of species abundance, which measures the degree to which species are equally represented in a community, was determined using Pielou’s J’ evenness (J’ = H’/lnS [41]). Graphical presentations of species frequency distributions to elucidate dominance patterns within communities were plotted in the form of k-dominance curves. These curves are cumulative ranked abundances plots, where the cumulative ranked abundance of each species is plotted against the species rank or logarithmic species rank, in order from most abundant to least abundant species [31, 351. The advantage of presenting distributional properties of a community in form of a rank abundance plot is that information on patterns of relative species abundances can be extracted without reducing that information into a single summary statistic, such as a diversity index. Multivariate methods are more sensitive to subtle changes in species composition and/or abundance than univariate measures, among other reasons because the latter can have very similar results although communities may differ in their taxonomic composition [62,63]. Large sets of species abundance data frequently include a high number of zero counts (45-86 % in the present study) and have highly-skewed abundance matrices. Therefore, they rarely meet assumptions underlying standard multivariate methods such as principal components analysis (PCA) [5, 93. The greatest flexibility concerning the assumptions made about data is offered by non-metric multidimensional scaling (MDS [30]), since it uses the rank order of dissimilarities or similarities between samples [9]. Thus, this ordination technique attempts to construct a configuration, in a specified number of dimensions, so that the rank order of the distances between samples in
428
K. Kriiger,
the configuration agrees exactly with the rank order of the matching (dis)similarities. A measure of how well the two sets of ranks agree is Kruskal’s stress formula 1 [30]. Another advantage of MDS is that it permits a choice in the definition of (dis)similarities between samples so that the (dis)similarity measure is not dictated by the mechanics of the ordination method but by relevant ecological assumptions [9]. MDS has recently been recommended for the multivariate analysis of ecological data (e.g. [9, 261). Examples of ecological studies where non-parametric MDS has been employed include Samways 1441, Gray et al. [15], Warwick et al. [64], Clarke (191 and references therein) and Wright et al. [68]. The MDS analysis was carried out on the mean abundances of species in the treatment and control communities using the Bray-Curtis coefficient [6, 111: loo
i IYij-YikI/ i=l
i i=
tYij+Yik)
(1)
sjk’
i
(4)
Sjk(i)
1
where
I
where yi is the abundance of species i in the jth or kth sample and p is the number of species. The index ranges from zero, where two samples are totally similar, to 100, where two samples are totally dissimilar, i.e. have no species in common. The Bray-Curtis index has a number of properties (e.g. choice of transformation, invariant to jointly absent species) that renders it most suitable for the comparison of community structure based on species abundance data (e.g. [9]). Species causing differences or dissimilarities between communities in the treatment and control paddocks were identified using the ‘similarity percentages’ procedure (SIMPER) as described by Clarke [9]. This procedure partitions the mean Bray-Curtis dissimilarity between all possible cross-regime pat pair combinations for each sampling day into contributions of each species and ranks them in order of their importance. The contribution of each species (6,(i)) to the dissimilarity between sample j and k is defermined as follows: lijk = 5 tijk (i)
Scholtz
the mean dissimilarity between two communities and thus is a good ‘discriminating species’. It has to be noted that the value of 1.4 is a subjective distinction. It has been chosen based on the fact that a mean-to-standard deviation greater than about the square root of 2 is indicative of a real effect, under normal distribution assumptions. However, the data are neither normally distributed nor independent. In a similar way species that are typical or characteristic of a community can be determined using the Bray-Curtis similarity S (Sj,=_loO - 4k.k)[9]. The mean contribution of a species (Si) to the similarity within a community is defined as the mean over all pairs of pats Cj,k) of the ith term Sjk(i):
i=
6jk=
C.H.
(2)
i= I
where
Sjk(i)= 2~minty,j~yik)/ i tyy+ Yik) i=l
The respective data for the two treatment and control paddocks were pooled for the analyses with the exception of the k-dominance plots. The dominance pattern for each paddock was plotted separately to determine if the treatments and control paddocks showed the same patterns. For the multivariate analyses, the original species abundance data were fourth-root transformed (Y”.25) to achieve a balance of contributions from rare and common species [9]. The species abundance data from natural pats, which varied in size, were standardized to relative abundance before fourth-root transformation. The programs to compute the Bray-Curtis coefficient and to perform the ‘similarity percentage’ analyses were written in SAS@ (SAS Institute Inc.). Nonparametric multidimensional scaling (MDS) was performed by the SAS procedure MDS [45]. Tests for significant differences between two samples for the Shannon diversity index were carried out on a spreadsheet (Microsoft Excel Version 5.0~). For the remaining analyses, the PRIMER (Plymouth Routines In Multivariate Ecological Research) [9] programs DIVERSE and DOMPLOT were used.
(3)
3. RESULTS sjk(i) averaged over211 pat pair combinations gives the mean contribution 6i from the ith species. A measure of how consistently a species contributes to the mean dissimilarity is the mean-to-standard deviation ratio. A large mean-to-standard deviation ratio (i.e. 8.i/SD6i > 1.4) indicates that a species contributes conststently to
In total, 42 422 specimens representing 88 species were processed. These include 48 Scarabaeinae and 14 Aphodiinae (Scarabaeidae), 11 Staphylinidae, 5 Histeridae, 2 Hydrophilidae, 1 Carabidae and 7 Diptera (Cyclorrhapha) species. Acta
Oecologica
429
Ivermectin and dung insect community structure. I
JFMAMJJASONDJFMAMJJASONDJF+fA
1991
1992
I
1993
I
Figure 2. Climate
diagram (after Walter and Lieth [61]) depicting the mean monthly temperature (Potchefstroom) and precipitation (Parys) for the period of January 1991 to March 1993. The dotted areas denote the arid periods (precipitation < evaporation) and the vertical lines denote the humid periods (precipitation > evaporation). Solid black areas denote the months receiving in excess of 100 mm on a reduced scale (1: 10).
3.1. Climate The rainfall before and during the rainy season (October to April) in 1992/93 was low except for November and December 1992 (figure 2). During the rainy season, rainfall was 96.5 mm below the mean of 520.5 mm (1904-1994). 3.2. Overall diversity The values for the overall diversity are shown in table I. The rainfall in the year preceding the trial was Table I. Overall 19920993
insect
in artificial
and naturally-voided
pats in treatment
(I) (P3 & P4) and control
(C) (Pl
& P2) paddocks
Season.
Time after treatment (months) Artificial
diversity
below average in the rainy season (October 1991 to March 1992, figure 2). In the summer rainfall region of South Africa, dung beetle activity usually reaches its peak in December and January when rainfall is high [lo]. As a result of the low rainfall prior to November, species richness was lower than expected for the pretreatment communities (December 1992). A comparison of the designated treatment with the designated control paddocks shows that species richness and H’ were lower in the former. The difference between the two types of paddocks with respect to H’ were signif-
Regime
Number
of individuals (n)
Species
richness (9
Shannon’s diversity (H’)
Evenness
(J’)
pats
pre-treatment 1 2 3
Naturally-voided 1
143
32
2.52
0.73
1 008
39
2.64
0.72
1 546
42
2.24
0.60
1 997
51
3.05
0.78
2 239
54
2.81
0.70
3 763
61
2.56
0.62
1 782
41
2.4 1
0.63
4644
65
2.15
0.66
4 214
45
1.46
0.38
60
2.17
0.53
58
2.41
0.59
59
2.86
0.70
55
2.43
0.61
69
2.94
0.69
pats 3 522 4 490 3 803
3
4 885 3 126
Vol. 19 (5) 1998
(n = 20).
K. Kriiger,
430 icant (H’: t, = 2.16, P < 0.05). However, J’ showed few differences between both types of paddocks (treatment, control). Rainfall was comparatively high during November and December (figure 2), and the number of species was higher in both treatment and control paddocks one month after treatment (January) for both artificial and naturally-voided pats compared with the pre-treatment. Similar to the conditions of paddocks before treatment, species richness was lower in treatment paddocks compared with controls. The differences in species diversity observed before treatment increased; H’ was highly significantly lower (P < 0.001) in treatment paddocks compared with the controls in both naturally-voided (t, = 18.27) and artificial pats (t, = 18.58). This difference could be a characteristic of the paddocks themselves and not be due to the ivermectin treatment of cattle. However, whereas H’ in the control communities increased, it decreased in the treatment communities in the artificial standardized pats. Comparably, species evenness, which was similar in both types of communities before treatment, increased in the control paddocks but dropped in the treatment paddocks relative to both the contemporary control and the pre-treatment communities. No clear pattern was evident two months after treatment because natural and artificial pats showed different trends for H’, J’ and species richness. Three months after treatment, H’ was highly significantly lower (P < 0.001) in treatment paddocks relative to the controls in both naturally-voided (t,= 17.51) and artificial pats (t, = 8.77); species richness and J’ were also reduced. Shannon’s diversity and J’ in artificial pats were also lower within the treatment paddocks compared with two months after treatment. 3.3 Rank abundance plots Figures 3 and 4 represent the k-dominance plots for artificial and natural pats. The most elevated curve corresponds to the least diverse community if the curves do not cross over. If the curves do cross, they are strictly speaking not comparable, because different diversity indices give opposing results [3 1J. The interpretation of the pre-treatment curves (figure 3) is hampered by the crossing-over of curves. The curves for P3 and P4 (I) cross over that of Pl (C) and are therefore not comparable. Paddock 2 (C), whose curve does not cross over those of paddocks P3 (I) and P4 (I), has the relatively least elevated curve and represents the most diverse community of the three. One and three months after treatment, the curves for the treatment paddocks lie clearly above those of the controls for both artificial and naturally-voided pats.
C.H.
Scholtz
100 y
90
22
80
w is s: OQ w 3 E
70 60 50 40
3 E
30
u
20 10
--
0
--,
+ x--El--P3, -P4,1
“‘PI, c -.P2,C I I
1
10 SPECIES
RANK
Figure 3. k-Dominance curves for dung insect abundance in artificial pats in the treatment (I) paddocks P3 and P4 and control (C) paddocks PI and P2 before injecting cattle with ivermectin.
This indicates higher species dominance and therefore a lower diversity in the treatment paddocks compared with controls (figure 4a, b, e, f!. Two months after treatment, the curves for natural pats show that treatment paddocks were less diverse than controls, whereas those for artificial pats indicate that the two types of paddocks had similar diversity @gure 4c, d). 3.4. Multidimensional
scaling ordinations
The non-metric MDS configuration for mean species abundance data of a community for all sampling dates in artificial and naturally-voided pats is presented infigure 5. The pre-treatment samples for artificial pats (standardized to relative abundances) have been included in the MDS analysis for natural pats to facilitate comparison of communities before and after treatment, because no pre-treatment sampling was carried out for natural pats. 3.4.1. Artificial
pats
Both the treatment and control communities changed gradually with time. The treatment communities were rather different from those of controls before treatment. The dissimilarity between the two types of communities increased one month after treatment. Two months after ivermectin therapy, the treatment communities were more similar to those of controls than one and three months after treatment. The dissimilarity between the treatment and control communities increased again three months after treatActa
Oecologicu
ivermectin and dung insect community structure. I
431
M
--
+
40 -30 --
+
20 --
+ x
10 --
eP3.1 --P4,1
-p4,1 0 10
Pl,C P2,C
1
10
(d) 100 90 -so -70 -60 -M
--
40 f
(eLl P g80 co 9
70
CQ E E
so 40
i
30
v
20
10 SPECIES
Figure 4. k-Dominance lines) paddocks. after treatment.
curves a, c, e: artificial
Vol. 19 (5) 1998
RANK
for dung insect abundance pats; b, d, f: naturally-voided
10
SPECIES
RANK
in artificial and naturally-voided pats in treatment (I, solid lines) and control (C, broken pats. a, b: one month after treatment; c, d: two months after treatment; e, f: three months
432
K. Kriiger,
C.H.
Scholtz
ment. These observations are in accordance with the results of overall diversity and k-dominance plots.
(a)
3.4.2. Naturally-voided
pats
The overall MDS configuration for communities in naturally-voided pats shows that the treatment communities were relatively different from their controls one month after treatment. In contrast to artificial pats, the two types of communities became gradually more similar two and three months after treatment. 3.5. Species analysis The artificial standardized pats are superior to naturally-voided ones for quantitative observations. Although naturally-voided pats may reflect pat colonization more realistically, this type of pat varied considerably in size (ca. 0.8-5 kg), and these differences exerted a strong influence on the colonization of pats. Therefore, emphasis was placed on artificial pats. Unless stated otherwise, species typical of a community and good discriminating species were found to belong to the Scarabaeidae (Coleoptera). The previous analyses have shown that some differences existed between the two types of paddocks before treatment. To assess whether the differences observed one and three months after treatment were due to ivermectin treatment or a reflection of differences between the paddocks themselves, the typical species for the respective communities were identified, as well as those that were responsible for these differences. The terms typical (characteristic) and discriminant species refer to those species that contribute to 70 % of the within-group similarity and 50 % of the between-group dissimilarity respectively. m
Figure 5. Two-dimensional non-metric scaling ordination of fourth root transformed mean species abundance data in artificial pats (stress =0.04, (a)) and of fourth-root transformed mean relative species abundance data in naturally-voided pats (stress = 0.03, (b)). Each point represents the communities in the treatment (tilled circle) and control paddocks (open circle) at a given time. BT: Before treatment; 1 m, 2m, 3m: one, two and three months after treatment. No values for the axes of the MDS plots are given, because such plots can be arbitrarily scaled, located, rotated or inverted as they show the relative position of samples to each other 191.
3.5.1. Before treatment Four species (12.5 %) in the treatment (I) and six species (15.38 %) in the control paddocks (C) were characteristic for the respective communities (i.e. treatment, control). Of these, two speciss (Euoniticellus intermedigs (Reiche),-Y, = 4.95, Y, = 15.00; Sisyphus sp. 1, Y, = 3.45, Y, = 1.45) were characteristic in both types of paddocks. Species that were mainly responsible for differences between paddocks before treatment were predominant either in the treatment or the control paddocks. Only one species contributed relatively consistently to this dissimilarity (Aphodius pseudolividus Balthasar) (table Ila). 3.52. One month after treatment (artificialpats) The communities changed with time and 10 species were characteristic of the control community com-
433
Ivermectin and dung insect community structure. I Table II. Mean abundance
(7 ) of dung insects in treatment paddocks (I) and controj paddocks (C) in artificial pats in 1992/93. Species are listed in decreasing order of importance in their contributions (6i ) to the mean dissimilarity (6 ) between treatment and control paddocks, with a cut-off of the cumulative percent contribution (X8; %) at 50 %. Dung beetles: T, telecoprid (ball-rollers that bury dung away from the pat); P, paracoprid (construction of nests in the soil beneath a dung pat); E, endocoprid (construction of nests directly in a dung pat); K, kleptoparasite (utilizes dung that has already been buried by para- or telecoprids). The affinity of suspected kleptopamsites is uncertain and these are listed under paracoprids. a) Mean dissimilarity
between
treatment
Species Aphodius
pseudolividus
Scarabaeoid
(E)
larvae
Aphodius
moestus
Euoniticellus
(E)
ajiiicanu.s
Onthophagus
(P)
sp. 12 (P)
and control Yl
before
treatment,
8 = 56.86
yc
Bi
6i/SD(6i)
0.70
4.40
3.67
1.51
6.46
5.05
5.60
3.49
1.07
12.60
8.25
3.80
3.10
1.15
18.05
0.30
I .50
2.85
1.39
23.07
X8;%
4.90
2.30
2.78
1.18
27.95
Aphodius
dorsalis
(E)
0.25
3.40
2.71
1.10
32.83
Liatongus
militaris
(P)
1.50
0.70
2.62
1.32
37.43
Aphodius
amoews
(E)
1.50
1.20
2.39
1.11
41.52
sp.10 (P)
0.35
1.65
2.3 I
1.05
45.58
1.10
1.80
2.15
1.03
49.36
&/SD@,)
ZBi%
Onthophagus Chironitis
scahrosus
(P)
b) Mean dissimilarity
between
Species
treatment
and control UT
one month
after treatment, 7,
8 = 58.88 8,
Diptera
sp.6
26.45
2.75
3.93
1.56
6.67
Diptera
sp.3
18.00
4.55
3.34
1.60
12.35
0.05
4.25
2.64
1.56
16.84
1.40
8.60
2.56
1.46
21.19
Colobopterus
maculicollis
Ohthophagus
sp. 12 (P)
Onthophagus Aphodius
gazella moestus
(E)
(P)
(E)
0.80
3.55
2.47
1.69
25.39
7.45
7.55
2.41
1.26
29.49
Sphnrridium
sp. I
0.60
3.95
2.25
1.41
33.30
Onthophagus
sp. IO (P)
0.30
3.15
2.21
I .37
37.06
3.70
3.45
2.09
1.26
40.6 I
Sisyphus
sp. I (T)
Aphodius
pseudolividus
(E)
2.10
7.60
2.08
1.25
44.13
qfricanus
(P)
0.40
2.50
1.99
I .28
47.5 I
Euoniticellus
pared with six in the previous month. In contrast, only half the number of species (i.e. 5) was characteristic of the treatment paddocks, compared with 4 for the pretreatment community. The number of typical species in the control communities increased to 19.61 %, but decreased to 11.90 % in the treatment communities. These results are indicative of a higher species dominance pattern in the treatment communities compared with controls, as also observed in the k-dominance plot cfigure 4a). Six discriminant species, which contributed relatively consistently to the differences between the two types of communities, were identified: Colobopterus maculicollis Reiche, Onthophagus gazella Fabricius, Onthophagus sp.12, Sphaeridium sp.1 (Hydrophilidae) with a lower abundance and Diptera spp.3 and 6 with a higher abundance in the treatment paddock-s compared with the controls (table Zb). This is in conVol. 19 (5) 1998
trast to the pre-treatment communities, for which only one species was consistently discriminant. 3.53. One month after treatment (naturally-voided pats) A comparison of treatment versus control paddocks for naturally-voided pats showed that only 0. gazella, which was l_ess abundant in the treatment paddock (YI = 1.00, Y, = 6.30) contributed relatively consistently to the intra-group differences. One beetle species that contributed to the dissimilarity between communities (C. maculicollis), was absent in the treatment paddocks in naturally-voided pats. Two fly species (Diptera spp.3 and 6), that had a high abundance in artificial (untreated) pats, appear to have dominated the communities in the treatment paddocks (table ZZ). However, these had low abundance in naturally-voided (treated) pats in the same paddock (Diptera sp.3:
434
K. Kriiger,
Table III. Mean abundance (y ) of dung insects in treatment paddocks (I) and control paddocks decreasing order of importance in thejr contributions (6i ) to the mean dissimilarity (6 ) between cumulative percent contribution (16, %) at 50 %. Dung beetles: T, telecoprid (ball-rollers (construction of nests in the soil beneath a dung pat); E, endocoprid (construction of nests directly has already been buried by para- or telecoprids). The affinity of suspected kleptoparasites is a) Mean dissimilarity
between
treatment
and control
two months
after treatment,
C.H.
Scholtz
(C) in artificial pats in 1992193. Species are listed in treatment and control paddocks, with a cut-off of the that bury dung away from the pat); P, paracoprid in a dung pat): K, kleptoparasite (utilizes dung that uncertain and these are listed under paracoprids.
6 = 52.94
Species Onthophrrgus
sp.2 (P)
1.oo
28.05
2.63
I.59
4.98
Onthophagus
sp. 12 (P)
6.65
60.50
2.56
1.67
9.81
Onthophagus
sp. 10 (P)
I .30
13.51
Aphodius
16.95
I .96
1.58
IO.15
I.55
I .93
1.36
17.16
sp.2 (P)
0.30
2.9s
I .73
1.56
20.43
sp. 1
5.90
2.75
1.69
1.23
23.63
sp. 13 (P)
0. IO
3.70
I .62
I .32
26.68
7.90
3.25
I.61
I.15
29.72
6.55
6.90
I .53
1.0X
32.61
3.95
4.20
1.52
I .20
35.48
7.05
0.10
1 .so
0.88
38.31
I .40
6.10
1.49
1.26
41.12
I .45
2.70
1.39
I.10
43.75
3.25
I .x0
I .37
1.21
46.34
I .65
I SO
I .35
1.21
4X.88
4.75
moestus
Cmcobius Sphaeridium Onthophagus
(E)
Aphodius
pseudolividus
Aphodius
russatus
Sisyphus
sp.1(T)
Diptera
(E)
(E)
hp.3 sp. 1 (P)
Carcobius Colobopterus
maculicollis
Onthophagus
gclzella
(E)
(P)
sp. 1 (E)
Aphodius
b) Mean dissimilarity
between
treatment
and control
Species
three months
VI
yc
6 = 56. I9 8,
30.65
7.40
2.67
I .2X
0tlthophagu.s
sp. 12 (P)
4.36
53.80
2.6 I
I.51
9.40
Onthophagus
sp. IO (P)
1.45
25.40
2.5 I
1.51
13.86
sp.2 (P)
0.25
4.00
2.1 1
I .I7
17.62
I .90
16.90
2.07
1.43
21.30
Aphodius
moestus
Onthophagus
sp. I (P)
Caccobius
anzoen~~.s (E)
Aphodius Sisyphus
(E)
after treatment,
0.25
2.30
I.91
1.50
24.7 I
0.20
4.40
1.x1
I .45
27.93
0.35
11.25
I.81
I.13
31.15
2.50
4.90
I .59
1.21
33.99
10.60
39.30
I .56
1.26
36.76
0.55
2.10
I .54
1.25
39.50
I .35
3.55
1.51
1.24
42.18
0.15
2.30
I .49
1.25
44.84
3.95
4.55
I .44
1.16
47.40
4.05
10.30
1.39
1.18
49.87
sp. I (T)
Aphodius
sp. 1 (E)
Aphodius
impurus
Aphodius
pseudolividus
Philonthus Aphodius Caccobius Sphaeridium Coiobopterus
(E) (E)
ap. rummu
(E)
viridicollis
(P)
sp. I maculicollis
11 = 0.65, Yc= Y, = 0.40).
(E)
0.01; Diptera
sp.6: Y,
3.5.4. Two months after treatment naturally-voided pats)
(artifiial
= 0.05,
and
In accordance with the lack of differences between communities two months after treatment, nine
(16.67 %) and ten (16.39 %) species were characteristic of artificial pats in treatment and control paddocks, respectively, indicating a similar dominance profile. With regard to artificial pats, four species contributed relatively consistently to the between-group differences. All four species were less (Onthophagus spp.2, 10 and 12, Caccobius sp.2) abundant in the treatment paddocks (table Ma). However, if naturallyActu
Oecologica
Ivermectin and dung insect community structure. I
voided pats are considered, no species contributed very consistently to differences between treatment and control communities. 3.55. Three months after treatment (artificial and naturally-voided pats) In accordance with the previous analyses, differences between the treatment and control community were also obvious in the species analysis. Eleven species (16.92 %) were characteristic of the control community, compared with six species (12.79 %) in the treatment community in artificial pats. This suggests an increase in dominance compared with the contemporary control community and also in comparison with the treatment community of the previous month. Six species made a consistent contribution to the intra-group dissimilarity and had a lower abundance in treatment paddocks compared with those of controls (Onthophagus spp.2, 10 and 12, Cuccobius sp.1, Aphodius amoenus Boheman, Sisyphus sp.1) (table Mb). With regard to naturally-voided pats, only one species, A. moestus Fabricius, which was more abundant in treatment paddocks than in the controls (Yt T= 92.05, Y, = 9.10), contributed consistently to between-group dissimilarity. The most abundant scarabaeine species during the trial was E. intermedius with a total of 4 198 specimens collected. This species was typical in all communities (treatment, control) at all sampling dates, its rank being between the first and fifth position for both artificial and naturally-voided pats. This species did not contribute towards the differences between the treatment and control communities with regard to artificial pats, nor did it make a consistent contribution with regard to naturally-voided pats. 4. DISCUSSION When interpreting the above results, it is important to bear in mind that disparities between different types of paddocks after treatment may be due to pre-treatment differences and thus simply reflect characteristics of the respective paddocks. Furthermore, even if the communities of the various paddocks had been similar prior to treatment, it would not be possible to attribute to ivermectin any differences observed subsequently without separating the intrinsic characteristics of the paddocks from the effect of the agent’s residues. To this end, the results of the various analyses are compared below. Before ivermectin therapy, the areas which were to serve as treatment paddocks supported a smaller number of species and Shannon’s diversity was lower Vol.
19 (5) 1998
435 than in the controls. Intuitively, one would expect that with improved weather conditions species diversity and evenness should increase, as observed in the control communities, even if to a lesser extent after treatment. Contrary to this expectation, species diversity, evenness and the number of typical species (as defined above) dropped and species dominance increased in the treatment communities in artificial pats. In addition, species diversity, evenness and the number of typical species was lower and species dominance higher in naturally voided pats one month after treatment compared with standardized artifical pats before treatment. This suggests that the changes one month after treatment within the treatment community and the differences to the control community are most likely due to the treatment of cattle with ivermectin. Few differences between communities in treatment and control paddocks were obvious two months after treatment, as artificial and naturally-voided pats showed contradicting results. Scholtz and Krtiger [46] considered that several factors could be responsible for the apparent recovery. One possibility is that recovery was caused by immigration of insects from areas surrounding the treatment paddocks. This assumption is weakened, however, by a renewed drop in diversity and evenness and an increase in dominance of some species in the treatment paddocks relative to the controls three months after ivermectin therapy. Hence, the recovery after two months is more likely due to emergence of beetles from the pre-treatment period and to recovery from sublethal effects. For example, Houlding et al. [24] found that although a single subcutaneous injection of abamectin initially reduced egg production and oviposition rate in Onthophagus binodis Thunberg females, this effect was not permanent. The above theory would also explain the differences between treatment and control paddocks three months after ivermectin treatment: the depressive effect in the treatment paddocks could be a reflection of the conditions one month after treatment, diminished by the emergence of insects from the pre-treatment period and possibly also from immigration of insects from neighbouring paddocks. The present study offered an opportunity to compare the results from single-species laboratory tests with those of a field investigation. Three common beetle species which occur in the trial area (Euoniticellus intermedius, Onitis alexis and Onthophagus gazella) have been involved in laboratory tests (e.g. [ 12,28,42, 501). In this study, 0. alexis, a crepuscular species which buries dung at considerable depths beneath pats (ca. 37 cm), was probably undersampled due to our sampling technique. Therefore, no trends for populations of this species could be observed. Single-species studies on the effect of ivermectin on 0. gazella have shown that injectable ivermectin
436 inhibited larval development for up to 21 days after treatment [42]. Sommer et al. [50] recorded significant reductions in mandibular and clypeal widths of surviving third-instar larvae of this species that had developed in dung excreted 16 days after treatment. 0. gazella did not contribute to differences between the pre-treatment communities. However, it was less common in treatment paddocks than in the control areas and made a high and consistent contribution to differences between treatment and control communities one month after treatment. Laboratory studies have shown that ivermectin is lethal to E. intermedius larvae for at least 14 days after treatment, reduces adult emergence for at least 21 days and prolongs larval development for 28 days after treatment [12, 281. Holter et al. [22] observed in a trial in Zimbabwe that E. intermedius preferred dung from cattle injected with ivermectin over control dung two and eight days after treatment when ivermectin concentrations in dung were high. However, during the present field study, E. intermedius, which was the most abundant species, contributed little to the dissimilarity between treatment and control paddocks, suggesting that the influence of ivermectin on their populations in the field was not marked. Since no attempt was made to monitor the immigration of insects from surrounding paddocks, it is not possible to clarify whether ivermectin had little effect on the population of this species or whether immigration of E. intermedius specimens from adjoining areas was responsible. Fincher [12] studied the effect of injectable ivermectin on the progeny of two species of Philonthus (Staphylinidae) in the laboratory. He showed that these predators were significantly affected only one week after ivermectin treatment of cattle with a standard injection (200 pg.kg-I). In agreement with Fincher’s findings staphylinid predators, although abundant as adults and larvae during the trial, contributed very little to overall dissimilarities between treatment and control paddocks. Finally, from the results of the present study, it appears that ivermectin affected the dung insect community for three months after treatment by decreasing species diversity and evenness. The normal commercial use of ivermectin is in the control and treatment of parasitism in livestock. The focus for (anthelminthic) prophylaxis is the young animal, which for epidemiological reasons is the class of stock most likely to benefit from such treatment. In the present study, the treatment regimen was a departure from that most commonly adopted in South Africa in that ivermectin was administered to the adult cattle, rather than to weaners or selected animals [ 131. The purpose of this was to expose the entire insect fauna within the treatment paddocks synchronously to
K. Kriiger, C.H. Scholtz
faecal residues. It is likely that when used more typically in young animals, any effects resulting from ivermectin therapy would be less pronounced. As it is believed that an organism already stressed by its environment is more likely to be affected by exposure to a pollutant [39], it seems plausible that the ecotoxicological effects of ivermectin during periods of drought are likely to be more severe than under more favourable weather conditions. Southern Africa is regularly affected by drought (see [58, 591) and the effects reported above therefore do not represent a special case. Acknowledgements We thank R.J. Coertze and A. Deacon, University Experimental Farm, Pretoria, for supplying the cattle whose dung was used for artilicial standardized pats. A. Uys and R. Stals assisted in the field, and M.J. Theyse, M. Swanepoel and A. Uys helped with extraction of insects from dung pats. S. E&My-Younga and M. Uhlig assisted with identification of species. M. v.d. Linde implemented the programs to compute the Bray-Curtis coefficient and to perform the similarity percentages procedure in SAS and assisted with the data analysis. A.B. Forbes, S.L. Chown, M. Kruger, S. Endriidy-Younga, J.W.H. Ferguson and two anonymous referees provided constructive comments on earlier versions of the manuscript and K.R. Clarke and R.M. Warwick are thanked for stimulating discussions. The work was undertaken with support from the Foundation for Research and Development, the University of Pretoria and the Mazda Wildlife Fund.
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Acta
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