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Data Paper (Biosciences)
Long-term seasonal dominance of the wasp Trihapsis polita Townes (Hymenoptera, Ichneumonidae) in the Brazilian Atlantic Forest
expand article infoBernardo F Santos, Alexandre P Aguiar§, Anazélia M Tedesco|, Julio C R Fontenelle
‡ Division of Invertebrate Zoology, American Museum of Natural History, New York, United States of America
§ Departamento de Ciências Biológicas, Universidade Federal do Espírito Santo, Vitória, Brazil
| Secretaria de Estado de Meio Ambiente e Recursos Hídricos, Cariacica, Brazil
¶ Instituto Federal de Minas Gerais, Campus Ouro Preto, Ouro Preto, Brazil
Open Access

Abstract

Background

The temporal dynamics of insect populations in tropical environments is highly complex and poorly known. Long-term seasonality studies are scarce, and particularly so for ichneumonid wasps (Hymenoptera Ichneumonidae). This study represents an effort to elucidate aspects of seasonality and forest succession in the Brazilian Atlantic Forest.

New information

We report on the seasonal and successional dominance of the ichneumonid wasp Trihapsis polita (Cryptinae). A long-term survey of Cryptinae was carried out in a protected area of Brazilian Atlantic Forest, in primary, tall secondary and low secondary forest areas. Specimens were collected during rainy season (RS) and dry season (DS) between 2000 and 2008, with total sampling effort of 4,095 trap-days. A total of 8,385 specimens of Cryptinae were collected, of which 6,655 (79.4%) belonged to T. polita. The occurrence of T. polita species was heavily concentrated in the RS, with abundance 148× higher than during the DS. Seasonal fluctuation was also detected for Cryptinae as a whole, but was two orders of magnitude lower. Sampling efficiency also varied widely among areas, with the peak of abundance at the tall secondary forest. The dominance of T. polita in secondary vegetation might be of general interest, as this type of forest is currently on the rise, due to unprecedented levels of human pressure.

Keywords

Malaise trap; parasitoid; phenology; outbreak; Trihapsis polita; secondary forest

Introduction

The temporal dynamics of insect populations in rainforests is highly complex and poorly studied (Hamer et al. 2005;Wolda 1988). Long-term studies of insect seasonality in the tropics are scarce, largely due the difficulty in maintaining long-term sampling and sorting (Grimbacher and Stork 2009). For Ichneumonidae, one of the largest insect families and a dominant component of tropical faunas, data are particularly scarce, deriving mostly from species that are easy to collect and identify (Gauld 2006). For Cryptinae, its largest and least studied subfamily, with 408 genera and over 4,500 species, there are no detailed studies of seasonality for any Neotropical taxon. Cryptines occur in all terrestrial environments and are mostly ectoparasitoids of pupae and prepupae of a wide variety of hosts, including moths, butterflies, beetles, social and solitary wasps.

Herein we report the seasonal distribution of a dominant cryptine species, Trihapsis polita Townes (Fig. 1). Trihapsis Townes is known from two Brazilian species, T. punctata Townes, and T. polita Townes, both described from a few specimens (Townes 1970). The genus seems to be restricted to the Brazilian Atlantic Forest, but is not frequently collected: a single specimen was obtained after an extensive collecting program in that region (Aguiar and Santos 2010). The hosts and other biological aspects of the genus are still unknown.

Figure 1.

Female Trihapsis polita Townes, habitus.

Sampling methods

Sampling description: 

Fieldwork was conducted over the course of eight years (2000–2008). In each year, one field excursion was conducted during the dry season (DS, July-August), and one during the rainy season (RS, October-November). Three Malaise traps (Townes 1972) were set in each site, aligned and 25 meters apart from each other. The traps were left operating for 4–5 weeks; the content of each trap was collected every 7 days and treated as a sample. Samples from the dry season of 2006 could not be accessed and were not considered.

Total sampling effort was 4,095 trap-days, 1,827 in the DS and 2,268 in the RS. Sampling efficiency is expressed as the ratio between number of specimens and number of trap-days. The number of collected specimens and sampling efficiency for T. polita were compared to that of all other Cryptinae combined in order to contextualize its relative abundance and to compare the temporal dynamics of this particular species to the “background” of closely related species in the area. All specimens are deposited in the entomological collection of Universidade Federal do Espírito Santo (Brazil). The full dataset is available as supplementary material (Suppl. material 1).

Geographic coverage

Description: 

The study was conducted at Parque Estadual do Rio Doce, a 36,000 ha protected area in the Brazilian Atlantic Forest, state of Minas Gerais. Three sites within the park were sampled (Fig. 2): (1) an area of primary forest (PF) with well-developed canopy, overspread high trees, abundant bamboo trees and well developed understory; (2) tall secondary forest (TSF), an elevated, steep area; (3) an area of low secondary forest (LSF), dominated by bamboos.

Figure 2.

Map showing the study area. A, Brazilian Atlantic Forest (green) with the location of Parque Estadual do Rio Doce highlighted (white triangle). B, Map of the study area, with the three sampled sites highlighted. PF, primary forest; TSF, tall secondary forest; LSF, low secondary forest.

Coordinates: 

19˚48’18” and 19˚29’24” Latitude; 42˚38’’30” and 42˚28’’8” Longitude.

Usage rights

Use license: 
Creative Commons Public Domain Waiver (CC-Zero)

Data resources

Data package title: 
Raw_data
Number of data sets: 
1
Data set name: 
Raw_data
Data format: 
Excel
Description: 

Original raw data: number of female and male specimens of Trihapsis polita and other Cryptinae in each collected sample.

Column label Column description
Area Sampled area by successional state. LSF, low secondary forest; HSF, high secondary forest; PF, primary forest.
Dates-Start Starting day for that sample, corresponding to the day when the Malaise trap sample corresponding was initially set.
Dates-End Ending day for that sample, corresponding to the day when the Malaise trap sample was collected.
Season Categorical variable indicating whether sample was collected during the dry season (DR) or rainy season (RS).
Cryptinae Number of specimens of Cryptinae (except T. polita) collected in that sample.
Trihapsis polita-Males Number of male specimens of T. polita collected in that sample
Trihapsis polita-Females Number of female specimens of T. polita collected in that sample
Total Total number of specimens of T. polita collected in that sample
Pluviosity (mm) Ammount of precipitation recorded during the week at which the sampling took place.

Additional information

Results and Discussion

A total of 8,384 specimens of Cryptinae were collected, of which 6,657 (79.4%) belonged to T. polita, and 1,727 (20.6%) to all other Cryptinae combined (Table 1). The overall sampling efficiency was 2.04. For T. polita alone, sampling efficiency was 1.62, and for all the other Cryptinae combined, 0.42. This quantitative superiority, however, was not uniform (Fig. 3). During the dry season (DS), T. polita represented only about 7% of the total Cryptinae collected. This situation was then drastically reversed in the rainy season (RS), when this ratio jumped to nearly 85%. The differences between dry and rainy seasons remain evident if the weekly totals are independently compared and are again clear if each week (Fig. 4) is compared separately, year by year.

Total number of specimens collected for T. polita vs. other Cryptinae in all areas (PF, primary forest; TSF, tall secondary forest; LSF, low secondary forest) and seasons (DS, dry season; RS, rainy season). Sampling effort was identical for all sampling areas, adding to 4,113 trap-days total, but different between seasons (DS=1,836, RS=2,277).

Specimens

%

PF

TSF

LSF

Total

DS

RS

PF

TSF

LSF

Total

Trihapsis polita

1956

4691

10

6657

36

6621

69.2

86.9

6.4

79.4

other Cryptinae

871

710

146

1727

416

1275

30.8

13.1

93.6

20.6

Total

2827

5401

156

8384

452

7896

33.7

64.4

1.9

100.0

Figure 3.

Mean number of specimens per sample (total of 3 traps; 195 samples/8 years), with standard error bars, comparing T. polita (Tp) with other Cryptinae (Cr) in three successional areas, primary forest (PF), tall secondary forest (TSF), and low secondary forest (LSF) (left chart), and in the dry season (DS) vs. rainy season (RS) (right chart). PERD.

Figure 4.

Total number of specimens collected in each sampling week (=each black & white bar pair, equivalent to 3 areas x 3 traps) for T. polita (white, first plane) vs. other Cryptinae (black, behind), along the sampled seasons (Day number of year, where DS=183–215, RS=286–322), discriminated for each year (0–1 = 2000–2008). Left wall (YZ axes) shows daily records of precipitation (cumulative values within each month), for all years (2893 records total); right wall (YX axes) shows average of precipitation for each Day number of year (each day = average of all years). Scale for number of specimens and precipitation (Y-axis) are identical.

For Cryptinae as a whole, sampling efficiency during the RS was 0.56, versus 0.25 in the DS, that is, 2.25× higher in the rainy season. The increase matches the observations of Kumagai (2002) for the Ichneumonidae in a preserved area in the Atlantic Forest, which tripled in number in the traps in the RS. This indicates that a two to threefold increase during the rainy season could be “normal” for Ichneumonidae as a whole. For T. polita, however, seasonal influence was higher by two orders of magnitude, with sampling efficiency rising from 0.02 in the DS to 2.92 in the RS – a 146× increase (Table 2).

Comparison of sampling efficiency during the dry season (DS) vs. rainy season (RS) in the three sampled successional areas. RS/DS, how many times larger was the sampling efficiency in the rainy season in relation to the dry season. Sampling effort was identical for all areas, adding to 4,113 trap-days total, but different between seasons (DS=1,836, RS=2,277). %, percentage of specimens.

T. polita

other Cryptinae

Area

%

DS

RS

RS/DS

%

DS

RS

RS/DS

Primary forest (PF)

29.4

0.03

2.55

82.2

50.5

0.37

0.85

2.3

Tall secondary forest (TSF)

70.5

0.02

6.16

251.4

41.1

0.26

0.72

2.8

Low secondary forest (LSF)

0.2

0.00

0.01

3.2

8.4

0.10

0.11

1.1

PERD Total

79.4

0.02

2.91

148.3

20.6

0.25

0.56

2.3

The seasonal dominance of T. polita in the park was not a happenstance: it occurred repeatedly through the years (Fig. 4), as evidenced by its nearly uninterrupted numerical superiority in the samples (Table 3), and by its presence in 47.8% of the individual trap samples from the RS, against only 9.2% for the DS.

Number of females and males of T. polita collected, as opposed to all other Cryptinae combined. % ♀, the percentage of specimens of T. polita that are females; % T. polita, the percentage of the total specimens that correspond to T. polita

Season, Year

T. polita

T. polita

other Cryptinae

% ♀

% T. polita

RS, 2000

695

648

173

51.75%

88.59

DS, 2001

0

3

64

0.0%

4.48%

RS, 2001

370

280

135

56.92%

82.80%

DS, 2002

6

6

129

50.00%

8.51%

RS, 2002

639

758

382

45.74%

78.53%

DS, 2003

3

6

82

33.33%

9.89%

RS, 2003

137

637

110

17.70%

87.56%

DS, 2004

2

3

34

40.00%

12.82%

RS, 2004

1084

606

150

64.14%

91.85%

DS, 2005

1

1

27

50.00%

6.90%

RS, 2005

131

49

142

72.78%

55.90%

RS, 2006

23

45

62

33.82%

52.31%

DS, 2007

1

1

60

50.00%

3.23%

RS, 2007

364

155

121

70.13%

81.09%

DS, 2008

1

0

59

100%

1.67%

Overall DS

14

20

455

41.18%

6.95%

Overall RS

3443

3178

1275

52.00%

83.85%

Total

3457

3198

1730

51.95%

79.37%

There was a distinctive quantitative difference among the three successional areas for the occurrence of both T. polita and other Cryptinae (Table 1). All differences discussed next are statistically significant (see confidence interval bars in Fig. 3). For other Cryptinae, the primary forest (PF) area had the highest abundance (871 specimens, 50.4% of the total), closely followed by the tall secondary forest (TSF) (710; 41.1%) and low secondary forest (LSF) (146; 8.5%). For T. polita, however, the TSF supported a much higher number of specimens (4,691; 70.5%), followed by the PF (1,956; 29.4%). The LSF was clearly avoided by this species, with only 10 specimens collected there throughout the study (0.15%).

Parasitoid wasps in general are most abundant in the rainy season, as compared to dry periods (Gauld 1991). However, this relationship remains insufficiently discussed and documented in the literature. The high level of dominance documented for T. polita has never been reported for any species of Ichneumonidae in natural areas, representing a noteworthy fact by itself. Previous faunistic studies of ichneumonid wasps in the Neotropics (e.g. Aguiar and Santos 2010; Guerra and Penteado-Dias 2002; Kumagai and Graf 2000; Kumagai and Graf 2000; Saaksjarvi et al. 2004) have never report any species as particularly dominating the collected samples. Considering that studies at the species level are scant for Ichneumonidae, the case for T. polita becomes of further interest, both because it is a rare study and because it signals that there is much still to be gained from studies on ichneumonid ecology.

The notorious success of T. polita in the tall secondary forest, as well as its distinct population dynamics in relation to other Cryptinae, suggest it may naturally act as a large-scale parasitoid in intermediate successional stages. This might also reveal to be of more general interest, now or in the future: this type of forest is predicted to increase in the 21st century due to industrialization and urbanization (Thomlinson et al. 1996), and yet, "there is still a tremendous need to understand and further refine our knowledge of ecological processes involved in secondary succession" (Guariguata and Ostertag 2001).

Acknowledgements

Rogério P. Martins (UFMG, Belo Horizonte) received BFS and AMT in a scientific visit and donated the material used in this study. Maria Célia L. Carreiro kindly helped to count the specimens. This project benefited from funding by the Conselho Nacional de Pesquisa e Desenvolvimento/CNPq (Processes 520031/98-9 and 926.656.810), Brazil.

References

Supplementary material

Suppl. material 1: Raw data
Authors:  B.F.Santos, A.P.Aguiar & A.M.Tedesco
Data type:  collecting records
Brief description: 

Original data, discriminated by individual trap-samples (585 records), presented as Python lists (compatible with R, and most other computer languages). All variables contain 585 items, with data corresponding according to position (index).