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High local species richness of parasitic waSPS (Hymenoptera: Ichneumonidae;

Pimplinae and Rhyssinae) from the lowland rainforests of Peruvian Amazonia

Article  in  Ecological Entomology · December 2004

DOI: 10.1111/j.0307-6946.2004.00656.x

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Ecological Entomology (2004) 29, 735–743

High local species richness of parasitic wasps

(Hymenoptera: Ichneumonidae; Pimplinae and
Rhyssinae) from the lowland rainforests of Peruvian
Amazonia
I L A R I E . S Ä Ä K S J Ä R V I 1 , S A M U L I H A A T A J A 1 , S E P P O
NEUVONEN2, IAN D. GAULD3, REIJO JUSSILA1, JUKKA SALO1
and ANDRES MARMOL BURGOS 4 1Zoological Museum, Section of Biodiversity and
Environmental Science, University of Turku, Turku, Finland, 2Kevo Subarctic Research Institute, University of Turku, Turku,
Finland, 3The Natural History Museum, London, U.K. and 4Universidad Nacional de la Amazonia Peruana, Iquitos, Peru

Abstract. 1. The parasitic wasp family Ichneumonidae (Hymenoptera) is of

great interest because it has been claimed that its species richness does not increase
with decreasing latitude.
2. No extensive studies of the family have been conducted in South American
localities.
3. Arthropods were sampled using 27 Malaise traps in the Allpahuayo–Mishana
National Reserve (56 000 ha) in the north-eastern Peruvian Amazonian lowland
rainforest. The total duration of the sampling programme was 185 Malaise trap
months.
4. Altogether, 88 species were collected. This is one of the highest local pimpline
and rhyssine species numbers ever recorded. A comparison with results from
Mesoamerica revealed that at equal numbers of individuals sampled, the number
of Pimplinae and Rhyssinae species in Peruvian Amazonia is at least twofold
compared with lowland locations in Mesoamerica and somewhat higher than in
the most species-rich Costa Rican higher altitude localities.
5. Non-parametric methods of estimating species richness were applied. These
suggest that additional sampling would yield a considerable number of new
Pimplinae and/or Rhyssinae species.
Key words. Amazonia, anomalous latitudinal diversity gradient, Ichneumonidae,
local species richness, lowland rainforest, non-parametric species richness
estimating, Peru.

Introduction especially the family Ichneumonidae have been suggested to

It is widely accepted that there are more species in the
tropics than in other parts of the world (Gaston, 2000;
Hawkins & Diniz-Filho, 2004); however, there are also
many exceptions to this general trend. Parasitic wasps and
Correspondence: Ilari E. Sääksjärvi, Zoological Museum,
Section of Biodiversity and Environmental Science, Department
of Biology, FIN-20014 University of Turku, Turku, Finland.
E-mail: ilari.saaksjarvi@utu.fi
be less species rich in the tropics and this observation has
prompted much interest (e.g. Townes, 1972a; Owen &
Owen, 1974; Janzen & Pond, 1975; Rathcke & Price, 1976;
Hespenheide, 1978; Janzen, 1981; Gauld, 1986, 1987, 1991;
Noyes, 1989a; Gauld et al., 1992; Hawkins et al., 1992;
Gauld & Gaston, 1994; Gaston et al., 1996; Sime & Brower,
1998; Bartlett et al., 1999; Horstmann et al., 1999).
The family Ichneumonidae is one of the most diverse
components of insect life in almost anywhere in the world.
They are parasitoids and their larvae live and feed on or in
the host individuals (for general descriptions of the family

# 2004 The Royal Entomological Society 735

736 Ilari E. Sääksjärvi et al.
see Gauld & Bolton, 1988; Gauld, 1991; Hanson & Gauld,
1995). Townes (1969) estimated that there could be about
60 000 Ichneumonidae species in the world, but because of
the poor knowledge of the tropical faunas the present inves-
tigators estimate that the size of the family could be higher
than 100 000 (Gauld, 1997). With this kind of species
richness the family is surely one of the richest, if not the
richest, animal families that have ever lived on Earth.
The absence of some groups of Ichneumonidae in the
tropics can be explained by the absence of their host
groups (Gauld, 1987), but many host groups such as
butterflies and beetles increase dramatically in species
number from temperate to tropical regions (Crowson,
1981; Robbins & Opler, 1997). Many hypotheses have
been offered to explain the pattern. According to the
resource fragmentation hypothesis (Janzen & Pond,
1975; Janzen, 1981) the populations and individuals of
tropical host species are too scattered and scarce to sup-
port populations of specialist parasitoids. Rathcke and
Price (1976) stated that because of the higher predation
pressure the immature stages of the parasitoids are more
vulnerable to predation, especially by ants, in the tropics.
Gauld (1987) proposed that higher levels of predation
should also affect adult stages. While searching sparse
host specimens tropical female parasitic wasps have to
spend a lot of time exposed and experience higher levels
of predation than their counterparts outside the tropics.
According to the nasty host hypothesis (Gauld et al.,
1992; Gauld & Gaston, 1994), tropical herbivores are
less available to the parasitoids as their temperate coun-
terparts because tropical plants contain higher amounts of
noxious secondary metabolites, which in turn are seques-
tered by herbivores and used for their own protection.
However, much more information needs to be gathered
from tropical areas before the existence and shape of
the ichneumonid anomalous diversity gradient can be
confirmed and explained (Noyes, 1989a; Horstmann
et al., 1999). There are several reasons that make compar-
isons of temperate and tropical samples a non-trivial task.
Tropical communities typically include a substantial pro-
portion of many very rare species and ichneumonids are no
exception (Noyes, 1989a; Gauld, 1991). Many species, espe-
cially koinobionts (see below), are very host-specific para-
sitoids of rare and low-density hosts (Janzen & Gauld,
1997). Also, there may be critical differences in variables
such as seasonality (Morrison et al., 1979) and habitat com-
plexity (Tuomisto et al., 1995) that need to be taken into
account. For these reasons, to obtain a reliable picture of
the species richness in the tropics the sampling effort may
need to be considerably higher than in the temperate region
(Morrison et al., 1979; Noyes, 1989a). It should cover all
seasons as well as large- and small-scale variation of habitat
types, which may be much greater than previously thought
(Tuomisto et al., 1995).
As was noted by Gaston and Gauld (1993), sound quan-
titative information on the ichneumonid species richness
in and outside the tropics remains limited. This is not
only important for understanding the spatial patterns of
# 2004 The Royal Entomological Society, Ecological Entomology, 29, 735–743
ichneumonid species richness, but it may also severely affect
the estimation of the magnitude of global species richness
(Gauld, 1991; Bartlett et al., 1999). Especially in the
Neotropics knowledge has been very fragmentary and
limited (Gupta & Gupta, 1984), and it has been very diffi-
cult to draw any general conclusions about the spatial
patterns of the ichneumonid distributions in this region.
It is believed that none of the diversity gradient studies of
the family Ichneumonidae has included South American
data. Also, it is important to note that the ichneumonid
fauna of any locality in the largest lowland rainforest area
of the world, Amazonia, has never been sampled in detail.
In fact, there is also a general perception that lowland rain-
forests have comparatively few ichneumonid species
(Townes, 1972a; Porter, 1978, 1982). Whilst this is true for
some groups in some sites, for example Ophioninae in
Brunei (Gauld, 1985), this is not a general tropical phenom-
enon, as the Asian patterns are not replicated in Central
America (I. D. Gauld, unpubl. data).
There are no large ichneumonid collections in Amazo-
nia, even in Belem, Manaus, or Iquitos, which are some
of the best studied sites in Amazonia (I. D. Gauld,
unpubl. data). As it is known that the Amazonian rain-
forests occupy an area equal to the size of Western
Europe, without good and representative samples it has
been impossible to say virtually anything about the
species richness of the Amazonian ichneumonid fauna.
However, some conclusions were drawn by Porter (1978,
1982) who claimed that the Amazon Basin is relatively
poor in ichneumonids. This conclusion is interesting
because at the same time Amazonian, especially Western
Amazonian, rainforests have been postulated to possess
the most diverse faunal and floral assemblages on Earth
(Gentry, 1988; Wilson & Sandoval, 1996).
During the last couple of years the Colombian and
Peruvian Amazonian ichneumonid faunas have been
sampled in more detail (Sääksjärvi, 2003; Sääksjärvi et al.,
2003, 2004). From these studies it has become clear that
there is a diverse and relatively unknown ichneumonid
fauna occurring in Western Amazonia. The main emphasis
of the present study is to provide initial insights into local
Amazonian Pimplinae and Rhyssinae species richness based
on a long-term sampling programme in heterogeneous and
diverse Peruvian Amazonian lowland rainforest.
It is clear that any insect sampling programme will yield
only a proportion of the species present in the community.
This must be especially true with tropical communities,
which are often very species rich and difficult to sample,
and any diversity study should consider the coverage of the
inventory. Therefore good ways of estimating the true spe-
cies richness based on the collected samples are needed. The
methods available are little understood and their behaviour
and efficiency needs to be tested with real data sets (Colwell
& Coddington, 1994; Silva & Coddington, 1996). Thus, in
addition to simply reporting the observed species richness,
non-parametric ways of estimating species richness will be
applied to the data. By doing this, an idea of how sufficient
the sampling programme was can be generated.

Materials and methods
Study organisms and identification of the parasitic
wasp samples
Efforts have been concentrated to the ichneumonid
subfamily Pimplinae because it has been widely used in
other similar studies (Gauld, 1991; Gaston & Gauld, 1993;
Bartlett et al., 1999) and is taxonomically and biologically
one of the best-known ichneumonid subfamilies (Gauld
et al., 2002b). The Pimplinae is also biologically very diverse
(Fitton et al., 1988; Gauld, 1991) and, after the revisionary
works of Gauld (1991), Gauld et al. (1998), and Gauld et al.
(2002a), rather well-known in the Neotropics. All this
makes it a very useful subfamily to be used in biodiversity
studies. For this study to be as comparable as possible with
the similar study of Gaston and Gauld (1993) on the Costa
Rican pimpline and rhyssine fauna, the subfamily Rhys-
sinae has also been included in the analysis. Together with
the subfamilies Poemeniinae and Diacritinae (not yet found
in the study area) these two subfamilies have often been
treated as a single subfamily Pimplinae (e.g. Townes, 1969;
Fitton et al., 1988), which is however, not a monophyletic
group and has been divided into separate subfamilies
(Eggleton, 1989; Gauld, 1991).
Based on their life strategy, parasitoids can normally be
divided into two broad categories – idiobionts and koino-
bionts (Askew & Shaw, 1986). Idiobionts kill or perma-
nently paralyse their hosts at the moment of oviposition
whilst koinobionts allow their hosts to continue developing
after attack. Idiobiont parasitoid larvae are usually able to
develop successfully on a variety of different hosts found
within a single type of niche or substrate (Townes, 1972a;
Askew & Shaw, 1986; Fitton et al., 1988; Gauld, 1991 and
references therein). The living conditions experienced by
koinobiont parasitoid larva are considered to be much
more demanding, as it has to resist the various defences of
an active host. For this reason koinobionts are often asso-
ciated with a higher degree of specialisation than idiobionts
(Askew & Shaw, 1986; Gauld, 1987; Hanson & Gauld, 1995
and references therein). These parasitoids tend thus to
attack hosts that are related to each other either ecologically
or phylogenetically (Shaw, 1994).
Of the two subfamilies studied, rhyssines are idiobiont
ectoparasitoids of coleopteran and hymenopteran larvae
living deeply concealed in wood, whilst pimplines are
biologically much more diverse (see below) (Fitton et al.,
1988; Gauld, 1991; Hanson & Gauld, 1995).
From the collected samples all ichneumonids were iden-
tified into subfamilies. Then all pimplines and rhyssines
were identified into genera and further sorted into mor-
phospecies. Hereafter morphospecies is referred to as spe-
cies. The specimens were sorted into morphospecies using
mainly characters in Gauld (1991) and Gauld et al. (1998).
Whenever possible males were sorted only after females, as
many reliable characters are found in the structure of the
ovipositor. Morphological variation suggests that some of
the species might be complexes of closely related biological
# 2004 The Royal Entomological Society, Ecological Entomology, 29, 735–743
High species richness of parasitic wasps 737
species. An emphasis was not made on identifying the
specimens into described species because there are no iden-
tification manuals available for the Amazon Basin and
because high intraspecific variation (Porter, 1978; Gauld,
1991) is known to occur in Neotropical pimplines and rhys-
sines (e.g. variation in the coloration of many widely dis-
tributed mimics depending on the most abundant model
species).
To describe assemblage structure, the species occurring in
the study area were divided into four categories according
to Gauld (1991):
1. Idiobiont parasitoids of deeply concealed host species
(into this category species with very long ovipositors
have been included, including all the species of rhyssine
genus Epirhyssa and the pimpline genera of the tribe
Ephialtini Anastelgis and Dolichomitus).
2. Idiobiont parasitoids of rather weakly concealed host
species [into this category species of the pimpline tribe
Pimplini have been included (Neotheronia, Nomosphecia,
Xanthopimpla, and Pimpla), as well as the ephialtine
genera Clydonium, Zonopimpla, and Amazopimpla
(Sääksjärvi et al., 2003)].
3. Pseudoparasitoids feeding in egg sacs, or on spiders
guarding sacs (representing only the species of the
pimpline genus Zaglyptus).
4. Koinobiont parasitoids of adult spiders (represented by
the following genera of the Sericopimpla genus-group
(Gauld et al., 2002b): Polysphincta, Hymenoepimecis,
Acrotaphus, Ticapimpla, and Zatypota).
Study area
The present study was conducted in the recently estab-
lished Allpahuayo–Mishana National Reserve (56 000 ha),
which is located about 25 km from the city of Iquitos,
Department of Loreto, Peru, between the black-water
river Nanay and the Iquitos–Nauta road (Fig. 1). Accord-
ing to the Holdridge (1967) classification the prevailing
vegetation is moist topical forest. The climate in the study
area is humid and hot, with a mean annual precipitation of
about 3000 mm and an average temperature of 26  C
(Marengo, 1998). The National Reserve lies between 110
and 180 m above sea level.
The rainforests existing near the city of Iquitos are
famous for their habitat heterogeneity (Whitney & Alvarez,
1998). Different forest types support endemic species,
unique communities of flora and fauna, and very high
species numbers (Gentry, 1977; Gentry, 1988; Vásquez
Martı́nez & Phillips, 2000; Vormisto et al., 2000). The soils
in the study area present a mosaic of patches varying from
very nutrient-poor white sand (forests growing on these
correspond to Amazonian caatinga forest or varillal, see
Anderson, 1981 and Encarnación, 1985) to clayey, reflect-
ing the geological formations of the surface (Räsänen et al.,
1998). Forests growing on different kinds of edaphic condi-
tions support differentiated flora and fauna (Whitney &
738 Ilari E. Sääksjärvi et al.
80°
Napo
Colombia
Ecuador
0° Iquitos
Allpahuayo–Mishana
National Reserve
Nanay
10°
Peru
Amazon
0 500 1000 km 0 25 50 km
70°
Fig. 1. Location of the study area in Peruvian Amazonia.
Alvarez, 1998; Vormisto et al., 2000). General descriptions
of the climate, geology, and vegetation of the study area are
given in Kalliola and Flores Paitán (1998).
Sampling methods
Sampling was done by Malaise trapping. A Malaise trap
is a tent-like structure made of fine mesh netting (Townes,
1972b; Gauld & Bolton, 1988). As insects fly into the trap
they are gathered to the highest point of the trap and fall
into a chamber containing a killing and preservative agent.
In this case the agent was 75% ethyl alcohol. The traps used
were manufactured by Marris House Nets (Richmond Park
Avenue, Bournemouth, U.K.) and have proven to function
well in tropical conditions (see Gauld, 1991; Hanson &
Gauld, 1995).
The trapping was done in two periods and altogether in
four locations. All collecting was carried out in the non-
inundated tierra firme rainforests. The first sampling period
was from August 1998 to January 1999 and included two
sampling locations. The first location was near the village of
Mishana near the black-water river Nanay and the second
near the Biological Station of Allpahuayo close to the
Iquitos–Nauta road. The second period was from January
2000 to January 2001 and included three locations near the
Iquitos–Nauta road (one approximately the same as in
1998).
Sampling procedure was similar during both sampling
periods and in all four different locations. Five traps were
placed in each location. Traps in each of the four locations
were placed in different kinds of forest types as follows.
Two traps were placed in forests growing on nutrient rich
clayish to loamy soil and three traps on forests growing on
nutrient poor white sand soil with differing humidity and
forest structure (canopy height). The traps were placed on
the supposed flying routes of parasitic wasps and were
emptied every 2–4 weeks.
# 2004 The Royal Entomological Society, Ecological Entomology, 29, 735–743
Unfortunately, many of the gathering chambers were
stolen or destroyed during the field studies, especially dur-
ing the latter sampling period. For this reason the number
of effective trap days varied between 105 and 363 days per
trap. The total sample size for all 10 traps in 1998 was 44
Malaise trap months. In the beginning of the 2000 field
period 15 traps were placed into the field study locations.
Of these traps 14 were located at the same place all the time
and their average collection size was nine malaise trap
months. One trap was stolen twice at the halfway point of
the study and after that two new traps were established at
two new sites. The average collection sizes of these three
traps were five malaise trap months. In 2000 the total
collection for all 17 traps was 141 malaise trap months.
The present data represents one of the largest malaise trap
samples ever collected in the Amazonian region.
Data analysis
To facilitate comparisons with other rather well studied
pimpline and rhyssine faunas in the Neotropics the species
number was plotted against the number of individuals
sampled at the locations as well as those from several locations
in Mesoamerica [Costa Rica (Gauld, 1991; Gaston & Gauld,
1993); Panama and Belize (Bartlett et al., 1999)]. The data are
presented at three spatial levels: for the whole study area, for
different study locations, and for individual trap sites.
To evaluate how adequate the sampling programme was,
different ways of estimating the true species richness were
applied to the data. Traditionally, species richness has been
estimated by fitting the observed frequency distribution of
species abundance classes to a log-normal distribution and
estimating the area under the curve behind the veil line
(May, 1975; Pielou, 1975; Magurran, 1988). However, this
procedure has been found to have some serious problems
and its use is not recommended in most cases (Colwell &
Coddington, 1994; Silva & Coddington, 1996). Instead the
use of non-parametric methods and extrapolation of the
observed species accumulation curve seem to be the most
promising approaches at present.
Preliminary analysis showed that extrapolation is not an
acceptable method with this data. In the study, the total
collection of a single trap was used as a sampling unit
and placing the traps in different habitat types resulted in
heterogeneity among samples (for a test of heterogeneity,
see Colwell & Coddington, 1994). Therefore the observed
species accumulation curve is not only a function of increas-
ing sampling effort, but also to some degree reflects the
dissimilarity in species assemblages among trap sites.
The non-parametric methods used were Chao1 and
Chao2 (Chao, 1984, 1987), abundance- and incidence-
based coverage estimators [ACE and ICE (Chao et al.,
1993; Lee & Chao, 1994; Chazdon et al., 1998)], and first-
and second-order jack-knife estimators (Burnham & Overton,
1978, 1979). In all of these estimators the important
information is thought to lie in rare species or species
with low incidence. For a comprehensive review and
 High species richness of parasitic wasps 739

definition of the estimators and procedures used here, see
Colwell and Coddington (1994).
The strategy is to pick samples randomly from the species
by samples matrix and count all these estimators for a
successively larger and larger sub-sample size. As the
samples accumulate and more and more information is
included, the estimators generally become more accurate
(Colwell, 1997). An estimator is considered to have given
a useful estimate of the true species richness if it reaches a
plateau as the samples accumulate. Because the behaviour
of the estimators is affected by the order in which the
samples are added to the species accumulation curve,
the order of adding samples is randomised 200 times,
and the estimators are calculated for the averaged
species accumulation curve. The analyses were done using
EstimateS software (Colwell, 1997).
Results
Taxonomic and biological composition
There are 12 Epirhyssa, four Dolichomitus, one Anastelgis,
35 Neotheronia, three Nomosphecia, one Pimpla, four
Xanthopimpla, one Clydonium, one Zonopimpla, two
Amazopimpla (Sääksjärvi et al., 2003), three Zaglyptus,
six Acrotaphus, eight Hymenoepimecis, three Polysphincta,
three Ticapimpla, and one Zatypota species in the sam-
ples. The assemblage structure of this fauna, together
with a comparison of some other well studied localities,
is presented in Table 1. In general, the biological composi-
tion of the pimpline and rhyssine fauna in the study area in
the Peruvian Amazonia is rather similar in comparison with
other known tropical study localities (see comparison in
Gauld, 1991), idiobiont parasitoids of weakly concealed
hosts being the most species rich group.
It is suspected that at least the species of the Camptotypus
genus-group, especially Zonopimpla, are under-represented
in the sample. This is the case in Costa Rica where moderate
numbers of new species are continually found although there
has been no increase in numbers of species of Neotheronia
(Gauld et al., 1998). This genus-group contains many species
that are very rarely collected (Sääksjärvi et al., 2003, 2004).

Altogether, 88 pimpline and rhyssine species were

collected in Allpahuayo–Mishana. This represents the mini-
mum figure for local species richness of the study area. A
comparison with results from Mesoamerica (Fig. 2) reveals
that at equal numbers of individuals sampled the number of
pimpline and rhyssine species in Peruvian Amazonia is at
least twofold compared with lowland locations in Meso-
america and somewhat higher than in the most species-
rich Costa Rican localities (Gauld, 1991; montane forests).
Note that the only Neotropical genus of the subfamily
Rhyssinae Epirhyssa is not included in the Belize and
Panama data (Bartlett et al., 1999). However, this does not
have any considerable effect on the results as there usually
are at most only a couple of Epirhyssa species present in
Mesoamerican study localities (see Gauld, 1991).
Species richness estimates
The species richness estimates given by different methods
(see above) are: ACE (101 species), ICE (100 species), Chao1
(105 species, SD 11.7), Chao2 (102 species, SD 11.2), Jack-
knife 1 (105 species, SD 4.4), and Jack-knife 2 (114 species).
The values of common diversity indexes to facilitate future
comparisons are: alpha (20.66), Shannon (3.69), and Simp-
son (26.55). It is immediately obvious, however, that the
values given by non-parametric estimators cannot be taken
as accurate estimates of the true species richness (Fig. 3).
Practically all estimators correlated with the species accumu-
lation curve through the sampling programme and showed
no sign of stabilising. This implies that additional sampling

100
90
80
70
60
50
S

40
30
20
10
0
1 10 100 1000 10 000
Number of individuals

Fig. 2. The Pimplinae s.l. (Rhyssinae, Pimplinae, Poemeniinae) species number (S) plotted against the number of individuals sampled in
Peruvian Amazonia (open symbols; this study) and in Mesoamerica [closed symbols (the size of symbol refers to the locations altitude: largest,
< 400 m a.s.l., medium, 400–1600 m a.s.l., smallest, > 2000 m a.s.l.); Gauld, 1991; Gaston and Gauld, 1993; Bartlett et al., 1999]. The data from
Peruvian Amazonia is presented at three spatial levels: for the Allpahuayo–Mishana area (circle), for different study locations (diamonds), and
for individual trap sites (small triangles).

# 2004 The Royal Entomological Society, Ecological Entomology, 29, 735–743

740 Ilari E. Sääksjärvi et al.

Table 1. The biological composition of the Pimplinae s.l.. faunas in three temperate and four tropical sites (modified from Gauld, 1991).
Numbers in parentheses indicate percentages of the total species number at sites. Original data: Finland (Jussila, 1984), England (Owen et al.,
1981), Poland (Sawoniewicz, 1986), Costa Rica (Gauld, 1991) and Peru (the present study). See text for life strategies.

Costa Rica

Finland England Poland Cacao Escazú Santa Rosa Peru

Kevo Leics Warsaw Allpahuayo– Mishana
Idiobiont parasitoids of 7 (36.8) 4 (22.2) 11 (39.3) 22 (32.8) 12 (25.5) 9 (23.1) 17 (19.3)
deeply concealed hosts
Idiobiont parasitoids of 7 (36.8) 5 (27.8) 10 (35.7) 30 (44.8) 25 (53.2) 18 (46.2) 47 (53.4)
weakly concealed pupae
or cocoons
Idiobiont ectoparasitoids 1 (5.3) 3 (16.7) 2 (7.1) 7 (10.4) 2 (4.3) 4 (10.1) 3 (3.4)
of spiders/pseudoparasitoids
of spider egg sacs
Koinobiont ectoparasitoids 4 (21.1) 6 (33.3) 5 (17.9) 8 (11.9) 8 (17.0) 8 (20.5) 21 (23.9)
of spiders
Total pimpliform species 19 18 28 67 47 39 88
at site

would probably yield a considerable number of new species
to the local pimpline and rhyssine list. The reason for the
increase of the estimates with increasing sampling effort is
that the proportion of singletons (species represented in the
sample by only one specimen) and doubletons (species repre-
sented in the sample by two specimens) remain very high all
the time (Fig. 3). The observed species accumulation curve
also seems to be far from reaching a plateau, but as noted
earlier, the shape of this curve must be interpreted with
caution because of the heterogeneity among the trap sites.
Discussion
The study shows that the local species richness of at least
some groups of ichneumonid parasitic wasps is very high in
120
100
Number of species
the Amazon basin. This result supports the findings of
Gauld (1991) and Gaston and Gauld (1993) of the high
local species richness of tropical pimpline assemblages. It
is believed that the local species richness of pimplines and
rhyssines reported in this study is one of the highest
reported anywhere around the world. Earlier, Gaston and
Gauld (1993) reported that, when corrected for area, the
species richness of Pimplinae (in its traditional sense, see
above) in Costa Rica was greater than that for other regions
recorded until then.
The high pimpline and rhyssine species richness in low-
land Peruvian Amazonia is contrary to previous assump-
tion of Porter (1978, 1982), who claimed that the south-east
Brazil (between 28 and 20 S latitude) is the most important
centre of diversification for the genus Epirhyssa and that the
Amazon basin is relatively poor in ichneumonids. From the
area of south-east Brazil he reports 13 species of Epirhyssa
while from this single study area (an area of couple of
hectares) 12 species were collected. According to the results
it is quite obvious that the previous assumptions of the

minor importance of the Amazon basin as a diversity centre

80
Jack2 for ichneumonids will prove to be wrong. It is suspected
Chao1 that the main reason for considering Amazonia poor in
60 ICE
Observed
ichneumonids has been that no sampling programmes
40 Singletons exhaustive enough have been conducted there before. For
Doubletons example, from the study of the genus Epirhyssa by Porter
20 (1982) it can be seen that the collection effort in South
America is heavily biased against the Amazon basin.
0 The results are also in contradiction to a more recent
1 3 5 7 9 11 13 15 17 19 21 23 25 27
study by Horstmann et al. (1999) who found only a few
Number of trap sites included species of pimplines from the lowland rainforest canopy in
Malaysia. However, as they also have indicated, their sam-
Fig. 3. The behaviour of selected species richness estimators as the
pling effort was by no means sufficient. In addition, Malaise
function of increased sampling effort. Jack2, second-order jack-
knife; ICE, incidence-based coverage estimator; observed, the
trapping was used in this study, whereas Horstmann et al.
observed species accumulation curve; singletons, species collected (1999) used canopy fogging, which is considered to be
only once during the study; doubletons, species collected twice rather ineffective in sampling ichneumonids (Noyes,
during the study. See text for references. 1989b) and which is also designed to collect individuals

# 2004 The Royal Entomological Society, Ecological Entomology, 29, 735–743


from quite different microhabitats compared with Malaise
trapping. It seems that Horstmann et al. (1999) failed to
collect almost all of the species that are commonly encoun-
tered in Malaise traps. For example, one Malaise trap in
Brunei collected many species of Xanthopimpla in about
four weeks (I. D. Gauld, unpubl. data) although very few
were found by Horstmann et al. (1999).
Based on the present work, it is obvious that sampling
tropical Ichneumonidae requires a lot of effort, even on a
local scale. With a total sampling effort of 185 Malaise trap
months, many species appeared to remain unsampled in the
Allpahuayo–Mishana National Reserve. On average 7.8
pimpline and rhyssine individuals were caught per one
Malaise trap month. One of the main reasons for the diffi-
culty in sampling tropical ichneumonids is their rarity, but
surely this is not the only reason.
Previous studies in the area show that the structure of the
vegetation depends on soil type (Vásquez Martı́nez &
Phillips, 2000). Soil type was used as the main cue to detect
habitat variation in the study as well. But so far there is
practically no information on what variables really affect
the small-scale distribution of ichneumonids within an
Amazonian lowland rainforest. Thus, it is possible that
some small-scale habitat types important for ichneumonids
were missed in the study and therefore ineffectively
sampled. It is very important to note that in the study it
was only possible to sample a small portion of the habitat
heterogeneity occurring in the study area. As was noted
before, the lowland rainforests close to the city of Iquitos
in the Peruvian Amazonia are famous for their extreme
habitat heterogeneity (Whitney & Alvarez, 1998).
As ichneumonids are strong-flying insects, it is likely that
some species very rare in the collection are representatives
of species that live in habitats that were not sampled during
the present study. For example, palm swamps and
inundated forest types are found within a few kilometres
from the trap sites and, on a larger scale, it is not known
what is the effect of the Andean foothills on the pimpline
and rhyssine species composition of the Amazon basin.
Porter (1978, 1982) reported the Andean cloud forests and
foothills to be one of the major diversity centres for
Epirhyssa and it is possible, even though the study area is
situated several hundred kilometres inside the Amazon
basin, that the centre of the geographical range of some
species in the sample lies actually in the Andean foothills. It
is also possible that there exists a sampling bias towards
some groups of Ichneumonidae when using Malaise traps
alone. For example, in the second most species rich genus
Epirhyssa, half of the species were represented by only one
or two individuals. These things together suggest that
Epirhyssa is very species rich in the area, but at the same
time poorly collected by Malaise traps (Porter, 1978) or the
species are very rare.
Why are there so many species in the Allpahuayo–
Mishana National Reserve? At least part of the question
could perhaps be explained with the very high number of
different kinds of habitat types occurring in the area
(Whitney & Alvarez, 1998). The varying physical structure
# 2004 The Royal Entomological Society, Ecological Entomology, 29, 735–743
High species richness of parasitic wasps 741
of different kinds of forest types provide a large number of
niches available for a large number of species. Because
several different kinds of forest types are situated in this
relatively small protected area, the area provides interesting
possibilities for comparative studies of floral and faunal
communities. In this kind of environment it can be ensured
that the differences between communities are due to local
ecological conditions, rather than geographical location. In
the National Reserve it has been demonstrated that plant
distributional patterns are closely related to local-scale dis-
tributional pattern of soil types (Tuomisto & Ruokolainen,
1994; Vormisto et al., 2000). A similar kind of study
comparing the distributional patterns of certain plant (pter-
idophytes, Melastomataceae, Burseraceae, palms) and
animal groups (pimpline and rhyssine ichneumonids) is
currently under preparation (Sääksjärvi et al., in prep.).
Acknowledgements
We would like thank the following persons for helping us in
many ways during the study: José Alvarez, Mario
Escobedo, Gerardo Lamas, Teotista Mafaldo, Petri
Martikainen, Mari Pohja, Manuel Reategui, Pedro Ramir-
ez, Sandra Rios, Kalle Ruokolainen, Pekka Soini, Tauno
Sääksjärvi, Anssi Teräs, Hanna Tuomisto, Varpu Vahtera,
Victor Vargas, David Wahl, Sondra Ward, and the villagers
in Mishana. We thank the following institutions for help
during the study: Universidad Nacional de la Amazonı́a
Peruana, UNAP (Peru), Instituto Nacional de Recursos
Naturales, INRENA (Peru), Instituto de Investigaciones de
la Amazonı́a Peruana, IIAP (Peru), Instituto Nacional de
Investigación Agraria, INIA (Peru), Universidad Nacional
Mayor de San Marcos (Peru), The Natural History
Museum of London (U.K.), University of Turku Amazon
Research Team (Finland), and Zoological Museum of the
University of Turku (Finland). This study was partly
supported by the Ministry of Education, Finland (Biolo-
gical Interactions Graduate School grant to I.E.S.), the
Entomological Society of Finland (travel grant to I.E.S.
and grant to S.H.), and the EC-funded Bioresource-
Programme (travel grant to The Natural History Museum,
London to I.E.S.). Marja Vieno checked the language. Two
anonymous referees and the Editor provided constructive
comments on the manuscript. We thank you all.
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